Fig. 1 -
Aerial view of the small
fishing village of East Dover, Nova Scotia, and surrounding area. A
predominantly granite shoreline with minimal coastal development, and no
major rivers or agriculture in the vicinity, this area is exposed to the
Northwest Atlantic Ocean and is affected by the southwest-flowing Nova
Scotia coastal current.
Fig. 2 - In recent years, green seaweeds
have become increasingly prominent in the lower intertidal zone of a
small, moderately exposed sand beach at East Dover, Nova Scotia. This site
is remote from coastal development.
Fig. 3 - Bright green Ulva grows on
low intertidal rocks in summer on a clean, exposed sand beach. Brown
perennial seaweeds have long been common here, but no green seaweeds were
visible at this site in the 1960s and 1970s. “Greeness” is rising on the
shoreline as well as in the coastal waters, where seasonal chlorophyll is
peaking at higher levels.
Fig. 4 - Unusually shrivelled, mature
Fucus, as compared to the heavier, bushier rockweeds observed at this
site decades ago, now shares rocky habitat with Ulva in the lower
intertidal zone of a very clean beach. The change in Fucus suggests
lowered fertility, while the new appearance of Ulva may be confused
with an opposite problem: a degree of eutrophication.
Fig. 5 - Profuse growth of Enteromorpha
is visible in the lower intertidal zone of a clean beach today. During the
1960’s and 1970’s, however, this green seaweed was not observed at this
Fig. 6 - Late summer in heavily
sewage-polluted Halifax Harbour, Nova Scotia, Ulva thrives and
maintains a deep green color. The appearance of a high intertidal barnacle
belt at this sheltered location suggests eutrophication.
Fig. 7 - Mid-summer in a clean sheltered
inlet, rockweeds and kelp deteriorate as green filamentous algae becomes
Fig. 8 - Laminaria in moderate
shelter in mid-summer with Cladophora. The low level of
pigmentation in the kelp seems to contradict the impression of high
nutrient loading that might initially be suggested by the profusion of
Fig. 9 - At Shad Bay, Nova Scotia, on the
near shore seabed, at 5 – 10 meters depth, a green haze obscures the view
of perennial brown seaweeds. The prevalence of this green algae has risen
during recent summers.
Fig. 10 - Attached masses of green
filamentous algae accumulate in summer in clean, semi-exposed shallow
subtidal areas that were dominated 3 – 4 decades ago by red Chondrus
Fig. 11 - Green filamentous algae growing on
bottom that previously supported a near-monospecific stand of Chondrus
crispus. Chondrus crispus is now shorter and relatively
bleached in comparison to plants that grew at this location in the 1960s
Fig. 12 - Attached green filamentous algae
in beds of Chondrus crispus extends into the low intertidal zone
where wave action prevents drying.
Fig. 13 - Codium fragile, with
pronounced development of colorless hairs, now commonly shares shallow
subtidal habitat with bleached (yellow) Chondrus crispus.
Fig. 14 - Codium fragile with
colorless hair development, a profusion of tan filamentous algae, and pale
kelp, occupy rocky subtidal habitat where larger, darker kelp and
Chondrus crispus dominated in the 1960’s and 1970’s.
Fig. 15 - A multitude of filamentous forms
of algae share habitat with the Laminaria species that dominated
this habitat decades ago. The Laminaria is now smaller, and
exhibits increasing “white rot” at the tips, which is associated with
insufficient nitrogen fertilizer and related to light exposure.
Fig. 16 - Rocky subtidal zone dominated in
past decades by perennial brown and red seaweeds, Fucus, Laminaria
and Chondrus crispus, is now increasingly overgrown by filamentous
algae. All perennial seaweeds show lowered pigmentation.
Fig. 17 - Subtidal Chondrus crispus
is now typically yellowed in summer, where decades ago it was seen to grow
in darker shades of red and brown, and many types of filamentous algae
share the rocky habitat. (shown with Jonah crab, Cancer borealis)
Fig. 19 -
Thin sheet-like annual
algae grow with pale Chondrus crispus, and various filamentous
forms, during early summer at a clean, moderately sheltered subtidal site.
Fig. 20 -
Pale, membranous annual
algae grows with green filamentous species, and very small Chondrus
crispus, at a location that supported commercially useful, thicker,
dark Chondrus several decades ago. There has been no recent seaweed
harvest or ice scour at this site.
Fig. 21 - A turf of Corallina officinalis
increasingly dominates shallow subtidal habitat that was strongly
dominated by Chondrus crispus several decades ago.
Fig. 22 - Red and green sheet-like algae
grow late in summer at sewage-polluted Halifax Harbour, Nova Scotia.
Perennial brown seaweeds, kelp and Fucus, maintain deep
pigmentation at this nutrient-enriched location.
Fig. 23 -
Late summer on a
wave-swept promontory of a granite island, standard horizontal zonation of
perennial seaweeds is seen: Fucus, Chondrus crispus, and
Laminaria. The intertidal appearance in this area differs from classic
expectations and from earlier observations, however, since no barnacles or
snails are now normally visible above the belt of Fucus. Also, the
extreme bleaching of Chondrus crispus in recent years – to white –
presents a stark visual contrast to the normal appearance of this area
several decades ago, when Chondrus crispus remained red-brown
throughout the summer.
Fig. 24 (large file) -
Rocky exposed shoreline
at Peggy’s Cove, Nova Scotia. Below the blackish upper band of Fucus
is a belt of Chondrus crispus, which shows a wide range of color
variation, ranging from dark purplish-brown to yellow-green, as the
picture is scanned from left to right. This color change correlates to
variable degrees of fertilization of this red seaweed. The topography of
this site causes wave-induced water movement to be markedly amplified
towards the left hand side of the photograph. The resulting effective
fertilizer subsidy supports darkly pigmented Chondrus crispus at
this location, which persists throughout the summer, in full sunlight.
Fig. 25 -
Yellowed bed of
Chondrus crispus growing at East Dover, Nova Scotia, at a location
that produced harvestable quantities of dark purplish-brown moss in the
1960s and 1970s
Fig. 26 - Bright yellow Chondrus now
shows below the dark rockweed zone on granite “White Island” at East
Dover, Nova Scotia. Exposed to a fair degree of wave action, Chondrus
crispus at this location maintained darker pigmentation throughout
summers in decades past.
Fig. 27 - Rocky subtidal areas exposed to
moderate wave action are dominated by Chondrus crispus, which has
become increasingly bleached over recent decades.
Fig. 28 - Corallina officinalis
increasingly dominates parts of rocky habitat that were previously covered
by Chondrus crispus. In this location, where constant wave action
prevents drying, Corallina officinalis survives at a higher level,
and maintains a deeper pink pigmentation than has been noted in areas with
lesser degrees of water movement (e.g. Fig. 21).
Fig. 29 - Lithothamnion covers a
Fig. 30 - Dark belt of mussel spat,
Mytilus edulis, in a bed of Chondrus crispus.
Fig. 31 - Juvenile Mytilus edulis
compete for space with Chondrus crispus, on a rock that was
previously dominated by a thicker, darker growth of Chondrus.
Fig. 32 - In Nova Scotia, the rocky
intertidal zone in areas with low wave exposure is normally dominated by
two types of brown rockweed, Ascophyllum nodosum (seen in
background) and Fucus (foreground).Marine animal life,
including marine mammals, may contribute to conditions that optimally
fertilize marine algae.
Fig. 33 - Ascophyllum nodosum, an
olive-coloured seaweed that produces yellow reproductive structures along
the length of the mature fronds.
Fig. 34 - Ascophyllum nodosum,
olive-green when healthy and well-fertilized, increasingly shows yellowing
that affects the length of the mature fronds.
Fig. 35 - Fucus species, including
subtidal specimens, are now observed to increasingly lose normal olive
pigmentation in mature tissue.
Fig. 36 - Ascophyllum nodosum growing
closest to a small sewage outfall (pipe visible) maintains dark
pigmentation in a sheltered inlet, as the bulk of nearby similar plants
Fig. 37 - Generalized yellowing of
intertidal Ascophyllum nodosum inside a sheltered inlet is
interrupted only where a small sewage outfall delivers added dissolved
nutrients (mid-section of the far shore).
Fig. 38 - A marked gradient of pigmentation
in Ascophyllum nodosum correlates to variable degrees of
fertilization mediated by water movement at Prospect, N.S.
Fig. 39 - High intertidal Ascophyllum
nodosum exposed to greater wave action, at left, shows darker
pigmentation than similar plants growing in relative shelter, at right.
Fig. 40 - Yellowed Ascophyllum nodosum
showing red spots, seemingly related to the drying effect of high wind at
low tide, observed during a summer (2001) with normal-to-cool air
temperatures in Nova Scotia.
Fig. 41 - Red patches appear strikingly
unusual in comparison to the normal appearance of rockweeds growing in
this clean, sheltered location in decades past. Ascophyllum nodosum
gives the appearance of having been burned with intense heat.
Fig. 42 - Red tissue damage, presumably due
to desiccation stress, in Ascophyllum nodosum, turns black before
the dead tissue sloughs off.
Fig. 43 - Red tips on yellowed
Ascophyllum plants die, presumably due to desiccation. Less exposed
parts of the seaweeds maintain normal olive coloration.
Fig. 44 -
Short-cropped stands of
Ascophyllum nodosum now cover intertidal rocks in a sheltered
inlet, where this seaweed grew to significantly greater lengths several
Fig. 45 - Fucus shows a reversal of
the spatial pattern of tissue damage, as compared to the related
Ascophyllum nodosum. Olive pigmentation is maintained at the tips of
Fucus, while proximal tissue progressively yellows, reddens, and
then dies. Internal translocation of nutrients toward the actively growing
tips of Fucus may relate to the greater health and resistance of
this part of the seaweed.
Fig. 46 - Sharply contrasting colours are
now observed between Ascophyllum nodosum and Fucus growing
in sheltered habitat in spring.
Fig. 47 - Larger specimens of Fucus,
such as were long harvested live to fertilize gardens, now appear greatly
withered in comparison to their appearance several decades ago when
growing at these same locations.
Fig. 48 - Fucus, growing low in a
sheltered rocky intertidal zone, now appears to have withered to a
‘skeleton’ while still attached to the rock. Vulnerablility to occasional
storm wave damage seems not to be a prime cause of death of mature
seaweeds growing in these sheltered areas today, as compared to
observations made several decades ago. Perennial Fucus seaweeds
seem now to be increasingly reduced to thin dark skeletons as a result of
Fig. 49 - Analogous to the mounting
“post-spawning mortality” that is increasingly killing marine fish in this
area, the survival of individual seaweed organisms for multiple years and
their undergoing multiple reproductive cycles seems to exert a severe
drain on the reserves of mature Fucus plants.
Fig. 50 - All species of Fucus found
in this area show the same pattern of accelerated breakdown of mature
tissue. With less buoyancy, when these seaweeds wash onto beaches they are
now more likely to become embedded in the sand, which is another pattern
that has been observed to be increasing in recent years.
Fig. 51 - Subtidal Fucus, growing
with bleached Chondrus crispus: the mature Fucus specimen
has become withered and a dark brown skeleton remains, while the younger
Fucus looks healthy. This parallels patterns recently observed in
marine fish stocks in Atlantic Canada, in which bigger, older fish starve
while smaller ones are still found in relatively good condition.
Fig. 52 - Boulders that have long been
covered with brown rockweeds still support them, but the prominent dark
thin ‘ribs’ of the mature Fucus is a new sight to the long-time
observer of this particular beach.
Fig. 53 - Sewage tolerant Fucus
evanescens growing in Halifax Harbour maintains deep olive
pigmentation into late summer, and shares habitat with larger specimens of
Mytilus edulis than those generally found in cleaner intertidal
Fig. 54 - Pale Fucus in late summer,
growing in very clean, clear water, is heavily overgrown by epiphytic
Fig. 55 - Ascophyllum nodosum growing
at a clean, shallow subtidal location, with bleached Chondrus crispus,
supports a heavy load of epiphytic macroalgae.
Fig. 56 - Shallow granite bottom, in a clean
sheltered inlet, now lacks coverage by perennial macroalgae that
previously persisted for many decades at this location (largely kelp).
Fig. 57 - Filamentous growths are
increasingly prominent in kelp beds, and kelp plants appear to be smaller
and less darkly pigmented than were similar plants growing at these
locations several decades ago.
Fig. 58 - A steep, subtidal rocky incline
inside the mouth of Leary’s Cove at East Dover, N.S., long dominated by
large Laminaria, as shown at left, has shifted significantly within
two years (2001 – 2003) towards smaller, more delicately structured
macroalgae, as shown at right.
Fig. 59 - Drift kelp showing dark brown
Fig. 60 - Drift kelp showing marked loss of
pigmentation as compared to decades ago when the same species commonly
washed ashore at this location.
Fig. 61 - Live kelp appears smaller and less
darkly pigmented than it did in the past. Many new filamentous algal
growths are evident.
Fig. 62 - “White rot,” characteristic of low
nitrogen availability in kelp, now appears to be increasingly prevalent in
natural kelp beds. Abundant filamentous algae thrive at this location.
Fig. 63 - Laminaria growing in sewage
polluted Halifax Harbour maintain deep brown pigmentation throughout the
year. These seaweeds are also heavily affected by filamentous epiphytes.
Fig. 64 -
Classic, high intertidal
“belts” of barnacles and mussels dominate in non-classic locations
(shelter) inside sewage-polluted Halifax Harbour, reflecting the effects
Fig. 65 - Near a major sewage outfall, a
sheltered high intertidal zone in Halifax Harbour is heavily dominated by
barnacles and mussels: true eutrophication.
Fig. 66 - Classic “barnacle belt” habitat,
such as this granite slope exposed to heavy wave action at Peggy’s Cove,
Nova Scotia, now do not support barnacle growth at previously reported
Decadal changes in
seaweeds in Nova Scotia, Canada:
A case of ‘pseudo-eutrophication?’
Nutrient enhancement of seawater has been widely
observed to favour the growth of fine annual seaweeds over the heavier
perennial varieties. An increasing biomass of these fast-growing
relatively short-lived seaweeds seems often to be readily accepted as
evidence of accelerated nutrient loading of the environment. However,
declining grazer pressure can also result in increased standing stocks of
ephemeral algae, and the finer macroalgal species enjoy a natural
competitive advantage over heavier perennial seaweeds under conditions of
lowered nutrient availability. These factors may obscure the accurate
diagnosis of changes in aquatic systems, especially when distinguishing
between nutrient shifts that might be occurring in opposite directions.
Surprisingly, several other “symptoms” normally associated with
eutrophication of coastal waters may also appear under the opposite
scenario, oligotrophication, which has been the subject of substantially
less scientific study.
Decadal shifting patterns in natural seaweed
communities in Nova Scotia include an increase in ephemeral algal
“bioindicators” of eutrophication, yet, paradoxically, simultaneous
patterns of physiological change in declining perennial seaweeds and
animal life suggest a contradictory conclusion: lowered seawater
fertility. ‘Pseudo-eutrophication’ refers to this appearance of classic
“symptoms of eutrophication” under a changing scenario that appears
ultimately to be driven by declining fertility. The changing patterns in
macroalgae in Nova Scotia have not been associated with climate change,
but have coincided spatially and temporally with a dramatic general
decline in the abundance of fish and other marine animal life. A causal
link between these changing patterns is explored.
Significant changes have occurred in populations of
intertidal and subtidal organisms between the 1960’s and 1970’s and the
present time, along the unpolluted, exposed rocky coastline of Nova
Scotia. While not documented by formal scientific monitoring, sustained
changes are readily apparent to long-time coastal residents. The
commercial value of Chondrus crispus obtained from wild stocks in
this area has been negatively affected, since the resource has recently
been found to be mixed with a variety of undesired species, and changes
have been noted in the quality of the colloid extract (pers. comm. A
Critchley). Declining trends in classically-dominant red and brown
perennial seaweeds have been observed by this author, concurrent with an
increasing abundance of opportunistic green macroalgal species, and a
variety of fine, filamentous types, often growing as epiphytes. Recent
photographic evidence (taken during 2001 – 2003) is provided here.
Initially, this suite of changes appears to be consistent with trends that
have been associated elsewhere with the anthropogenic increase in nutrient
loading of coastal waters.
“…slight to medium eutrophication is therefore
characterized by increasing blooms of “nutrient opportunists,” in
particular fast-growing epiphytic macroalgae and bloom-forming
phytoplankton taxa. In contrast, phanerogam and perennial macroalgal
communities gradually decline, usually combined with a change in their
depth distribution limits, and finally disappear.” (Schramm 1996)
Seeming to confirm the impression of “slight to
medium eutrophication,” certain phytoplankton blooms have become more
prominent in the coastal waters of Nova Scotia in recent decades. This
includes a rising “greenness” indicator (chlorophyll a) during the
“spring bloom” (DFO 2003a), and, in keeping with a global trend, a rising
frequency and extent of “red tides.” Seagrasses are also observed to have
declined and been lost from many affected locations over recent decades.
While the declining pattern in perennial seaweeds
seems to have included a contraction of depth distribution, this is
difficult to establish due to a lack of historical records. More easily
observed is a pattern of range contraction in perennial seaweeds in which
they are increasingly lost, and seem to experience accelerated rates of
natural breakdown, in areas where the natural availability of plant
nutrients is lowest. Typically this is observed in sheltered inlets
receiving minor degrees of terrestrial runoff or direct human impact.
Patterns of physiological change in perennial macroalgae growing in clean,
sheltered areas seem to offer evidence contradictory to the
“eutrophication” hypothesis. Fucoid seaweeds, Chondrus crispus, and
kelps now show lowered pigmentation, stunted growth, and accelerated
breakdown in relatively sheltered areas, as compared to the appearance of
these species at the same locations three or four decades ago (personal
observation: unfortunately, no useful baseline photography or other
records were found.) In areas with relatively enhanced nutrient
availability, due either to greater degrees of wave action or to greater
input of terrestrial runoff, these red and brown perennial seaweeds appear
to be maintained in better health (deeper pigmentation, attaining larger
plant sizes, and greater resistance to breakdown by environmental
stressors such as temperature, light and desiccation).
The shallow coastal areas described here (shown in
Fig. 1) are generally well flushed, terrestrial runoff is low,
semi-diurnal tidal amplitude approaches 2 meters, and the region is
affected by the cold, southwest-flowing Nova Scotia current. Water
originates from areas to the north, the Newfoundland-Labrador shelf and
the Gulf of St. Lawrence (Breeze et al. 2002), two regions that have,
along with the adjacent Scotian Shelf, experienced massive declines in
fish abundance during the four decades which the observed seaweed changes
The primary determinant of the nutrient regime
available to the Nova Scotian seaweed communities described here appears
to be input from coastal oceanic waters overlying the Scotian Shelf.
Changes suggesting a decline in nutrient availability to these seaweeds
warrant investigation, since the implied decline in primary productivity
in the coastal ocean may relate importantly not only to the potential
commercialization of seaweeds, but also to problematic declines in other
local marine life: for example, the unexplained, ongoing poor condition
and failed “rebuilding” of commercial fish stocks (DFO 2003a).
It is suggested that seaweeds, especially perennial
forms, may serve usefully as bioindicators of a lowering of seawater
fertility (oligotrophication) as well as signaling the more commonly
described and suspected eutrophication of coastal waters, and that,
lacking a careful differential diagnosis, the former may surprisingly be
mistaken for the latter. Hence, the designation of this pattern here as
Assessing decadal patterns of change in coastal marine life
Changes in coastal marine life in Nova Scotia over
the past four decades have been so pervasive that it is virtually
impossible to find an unaffected (and easily observed) species.
Observations of multiple species, plants and animals both, must be
considered together to form the clearest, best-informed picture
(Stephenson & Stephenson 1972). However, for the purpose of discussion it
becomes necessary to some degree to consider them separately.
Beyond the observation of whether a given species is
“present” or “absent” in an environment, it is important to note any
changing trends in the physiological condition of individual organisms.
While shoreline organisms have generally not been monitored in this level
of detail (Bates et al. 2001, Schramm & Nienhuis 1996), this caveat is now
known in the assessment of marine fish stocks, where a high abundance of
small fish, which might be in fairly good condition, does not reveal the
quality of important changes that may be affecting the population as a
In recent years it has often been noted in Atlantic
Canadian fish stock assessments that fair numbers of healthy juveniles can
be maintained even as the age structure of the stock as a whole contracts,
in the absence of fishing, with the oldest fish increasingly losing
condition and succumbing to natural mortality (FRCC 2003). Reproductive
demands appear to take an increasing toll, as mortality related to
post-spawning exhaustion affects ever-younger fish. These two broad
patterns in marine fish species appear to be echoed today, if rather
subtly, in multiple non-commercial organisms, even including perennial
The young, and the short-lived, seem able to be
maintained longest under a scenario of dwindling resources in a marine
setting. This tendency has been confirmed by at least one modeling study.
Changes in a population of bivalve molluscs (Crassotrea virginica)
were modeled under a scenario of dwindling phytoplankton availability (in
Galveston Bay, U.S.A), and only a single early demographic change emerged:
no decline was found in oyster abundance, nor in coverage of habitat, but
the one change predicted was a lowering of the maximum size attained by
the oldest oysters (Powell et al. 1995). This signal in sessile
invertebrates, of early population starvation only subtly limiting the
survival of the largest individuals, agrees remarkably well with the broad
pattern that has emerged from Atlantic Canadian fish stocks, as the oldest
age groups of fish exhibit increasingly acute degrees of starvation. This
pattern may be characteristic of organisms that continue to grow in size
after reaching maturity, and seems also to be echoed in changing patterns
observed in intertidal organisms in general, seaweeds included.
Longer-lived, unexploited marine organisms, of both plant and animal
species, are growing to significantly smaller sizes along the Nova Scotian
coast than they did in the past. A generalized shrinking pattern seems to
have affected everything from snails, mussels and starfish, to rockweeds,
kelp and Chondrus crispus (personal observation).
Despite great natural variability in the morphology
and other growth characteristics of seaweeds, a certain consistency can be
expected at any given location within a predictable, steady environmental
regime. Barring the occasional massive removal by ice scour, a canopy of
perennial brown and red seaweeds, arranged in a pattern of horizontal
bands, normally forms the dominant feature of a stable “climax community”
on temperate zone rocky shores such as those of Nova Scotia (Stephenson &
Following is a description of changing trends in Nova
Scotian seaweed communities that have been familiar to this author since
the early 1960’s. Recent photographs are compared with personal
recollections of how seaweeds appeared at these locations in the past.
Unfortunately, no scientific time-series data exists on these, or other
similar seaweed communities, that might support or contradict the
observations made here. Beyond the gradual shifting patterns that are
evident to the long-time observer, many of these photographs illustrate an
apparent paradox of short-lived, fast-growing macroalgae (“symptomatic” of
eutrophication, or “overfertilization”) flourishing alongside heavier,
perennial seaweeds that are exhibiting stunted growth and lowered
pigmentation (characteristic of “underfertilization”).
Comparisons are made between changing patterns on the
open shore, and those seen in similar intertidal organisms living inside
heavily sewage-polluted Halifax harbour (which receives the untreated
wastewater from 400,000 people and is located on the same coastline).
Similarities and differences are described between known eutrophication
(inside the harbour) and the scenario of ‘pseudo-eutrophication’ (which is
suggested to be the reverse problem) that appears to be developing on the
clean open coast. Figure 1 shows the coastal region, in the vicinity of
East Dover, N.S., exposed to the open Northwest Atlantic Ocean and
situated 25 km southwest of Halifax Harbour, where the majority of the
photographs were taken. Others were taken along the shorelines of a few
small, uninhabited granite islands that are nearby, but were excluded from
the view in Figure 1.
Increased abundance of “opportunistic” seaweeds: greens and
The proliferation of short-lived green macroalgae
(commonly species of Ulva, Enteromorpha, and Cladophora)
has been strongly associated with, and considered to be a “bioindicator”
of, increased nitrogen availability in the environment (Schramm & Nienhuis
1996). While not building to the level of “green tides” reported
elsewhere, there has been an increasing trend in the appearance of these
delicate green seaweeds along the Nova Scotian coastline. Some extent of
formation of “green tide mats” has been observed during a recently
implemented effort to monitor seaweed diversity in the nearby Bay of Fundy
(Bates et al. 2001), although no trend has yet been documented. An often
prominent, bright green and “eye-catching” feature of intertidal and
subtidal zones today, these green seaweeds were relatively inconspicuous
in the past (to the point of appearing to be absent to the casual
observer). Rocks in the lower intertidal zone of a clean, exposed beach
visibly supported only heavy brown and red seaweeds decades ago (1960’s
and 1970’s, personal recollection) but an unmistakable and increasing
presence of ephemeral green macroalgae now colonizes them as well (shown
in Figures 2, 3,
4 & 5). Ulva species predominate, and these also
are seen to grow heavily, but in a deeper green, in sewage-polluted
Halifax Harbour (Fig. 6). Although water clarity in summer is generally
good along the open coast, a green haze, consisting in part of a
substantial presence of Cladophora species, increasingly obscures
the summertime view of perennial seaweeds inhabiting the shallow subtidal
rocky bottom of less exposed areas (Figs. 7,
8 & 9).
More firmly attached green filamentous species
increasingly grow among subtidal beds of Chondrus crispus (Figs.
& 11) where water movement is somewhat greater. Where wave action prevents
drying, these green growths sometimes extend up into the lower intertidal
region (Fig. 12). Three decades ago in summers, this author harvested
Chondrus crispus from these exact locations. Besides a larger, more
darkly pigmented growth of Chondrus normally developing on these
subtidal and intertidal rocks during those years, no green seaweeds were
visible in the moss beds.
Over the last 10 to 15 years, the previously absent
perennial green seaweed, Codium fragile, has increased in abundance
in this region. Some writers have suggested that Codium fragile
shares the high nutrient affinity characteristics of the “pioneering”
delicate green annual seaweeds (Romero et al. 1996) and may similarly
increase its growth in response to increased nitrogen loading of the
environment (Haritonidis 1996). The rise in Codium fragile on this
Nova Scotian coastline may therefore also seem to suggest part of a
community response to nutrient pollution. However, it may be that, due to
the ability of Codium fragile to scavenge a relatively greater
number of nitrogen species, its symbiotic relationship with a
nitrogen-fixing cyanobacteria, and its ability to grow a profusion of
colorless hairs to enhance nutrient uptake (Lobban & Harrison 1994), that
Codium has a competitive advantage over perennial species of red
and brown seaweeds under a scenario of declining nutrient availability.
Codium with pronounced hair development is frequently seen to share
subtidal habitat with pale, seemingly nutrient-stressed, red and brown
seaweeds, and with a variety of delicate filamentous species (Figs.
Besides the rise in the abundance of green seaweeds,
a multitude of filamentous species of various colors is becoming
increasingly prominent (Figs. 15,
18), along with a variety of
thin, sheet-like species (Fig. 19,
20) and a growing profusion of erect
Corallina officinalis (Fig. 21). Sheet-like annual algae are also
observed to grow profusely in polluted Halifax Harbour, where
comparatively deeper pigmentation is maintained (Fig. 22).
Chondrus crispus: changes in a dominant red
The most strikingly visible seaweed change has been a
long-term change in the summertime color of Chondrus crispus. Beds
that normally supported thick brownish-purple plants in summers, in the
early 1970’s, now produce smaller, green-yellow Chondrus plants
that sometimes bleach to white. (Figs. 12,
23) For over 150 years, this
common red seaweed has been reported to “bleach” (turn from red to green)
when growing in suboptimal habitat (stressed by high light and low
nutrient availability; initially this seems to have been noted only
occasionally, in extreme situations, such as in tide pools near the high
water mark (Harvey 1846-51)). The color change in Chondrus crispus
noted over the last three decades in Nova Scotia may be part of a
longer-term trend toward increased bleaching of this species (MacKenzie
2003a). Chondrus crispus still maintains dark brown, red, or purple
shades in areas where greater water movement augments fertilization, even
in full sunlight. The color gradient is shown in Fig. 24, at Peggy’s Cove,
N. S., where the topography of the shoreline causes water movement due to
wave action to be amplified toward the left hand side of the photograph.
The shifting trend in pigmentation, from darker purple-browns to lighter
yellow-greens, as the viewer scans the Chondrus belt from left to
right in Fig. 24, approximates the summertime change that has been
observed by this author over the past three decades in the moss beds
pictured in Figs. 12, 25, &
Green fronds of Chondrus crispus are
significantly less productive than red fronds (Harvey & McLachlan 1972);
therefore, the observed color change appears likely to signal a lowering
of the primary productivity of this seaweed along this Nova Scotian
coastline. While the percent coverage of the species may not have changed
greatly, Chondrus plants are visibly smaller and increasingly
bleached, reflecting a negative change. Decreasing plant size and
increased bleaching suggest an underlying dynamic which might not become
apparent with a program of monitoring only for the presence of species and
the extent of the area they cover. Since Chondrus crispus has
always bleached in suboptimal habitat while maintaining dark colors in
optimal habitat (MacKenzie 2003a), it seems less likely that a change in
the quality of light has triggered the trend toward increased bleaching,
than that a change in the nutrient content of the seawater has occurred.
Beyond the color change and the increased occurrence
of fine filamentous algae growing among the Chondrus crispus plants
(Figs. 12, 18), a further observed change has been a tendency towards the
replacement of Chondrus crispus by Corallina officinalis.
Coralline algae have classically formed a pink, crustose understory below
the canopy of Chondrus in this region, but, especially at subtidal
sites with moderate water movement, Corallina officinalis is now
increasingly forming a turf that replaces the generally bleached
Chondrus. Areas supporting a mosaic of the two species have tended in
recent years towards a relatively greater coverage by Corallina.
(Compare Figs. 27 and 21) The lower depth range of Chondrus
seems thereby to be receding.
Corallina officinalis has been variously
reported elsewhere to have increased in association with nutrient
pollution (Scotland: Fletcher 1996), been tolerant of such pollution
(Adriatic Sea: Munda 1996), and to have declined in association with
effects of eutrophication (Kattegat and Oslo Fjord: Wallentinus 1996). It
is therefore impossible to draw conclusions based only on a rising
dominance of Corallina. Corallina turf in this region appears
generally in a very pale pink color, often bleaching to white, and this is
presumably due to high light exposure as the larger seaweed canopy has
disappeared. However, reminiscent of the pattern in Chondrus crispus
(Fig. 24), a deeper pink color is maintained in Corallina growing
in full sunlight where water movement, and therefore fertilizer
availability, is relatively greater (Fig. 28).
Another change in red coralline algae has been
observed: a heavier, knobbly encrusting algae, a species of
Lithothamnion, that was once commonly found in this area, is now much
less commonly seen. When found today, this species of coralline algae is
now observed to grow to a smaller size than was seen in the past. An
example is shown in Fig. 29 of this species (covering the shell of a
periwinkle), which commonly grew in a substantially heavier form on subtidal rocks in this region decades ago. Within the corallines, the
theme seen in fleshy red and brown macroalgae therefore seems to be
repeated: a shifting trend away from the heavier species and towards those
with finer structures.
Occasionally, wave-swept intertidal beds of
Chondrus crispus are seen today in this region to be heavily covered
in patches with the spat of blue mussels, Mytilus edulis (Figs.
and 31). Not noted in decades past, when this author harvested the
Chondrus, this apparent increase in the range of small juveniles of
Mytilus belies the marked decline in larger members of this species
that has occurred in the area. A substantial decline in the population of
mussels growing to larger sizes has occurred in this region, and mussels
are now absent from much intertidal and subtidal habitat that once
supported them (MacKenzie 2001).
Changes in perennial brown seaweeds: fucoids
Superficially, there appears to have been little
change in fucoid seaweeds in this region: their dominant coverage of the
rocky intertidal zone continues, as shown in Fig. 32, except in areas of
extreme wave exposure, as has often been noted to be “normal.” (Stephenson
& Stephenson 1972). However, subtle, long-term negative changes can be
seen in populations of long-lived brown seaweeds, in Fucus species
in which individuals may survive for four or five years, and in the
dominant Ascophyllum nodosum, which may live for many decades.
When healthy, both types of “brown” seaweed are
generally of a dark olive green color, which darkens almost to black when
partly dried by exposure to air during low tides. Fucoid seaweeds divert
substantial resources into the annual growth of reproductive structures,
which are ultimately shed. It has been commonly noted that the
reproductive structures of fucoid algae grow to be less deeply pigmented
than the main body of the plant, and that they thereby take on a yellow
color. The normally contrasting green and yellow coloration of the
reproductive stage in Ascophyllum nodosum, shown in Fig.
long been noted by naturalists (Harvey 1846-51). What has not been
classically described, but is becoming increasingly prominent in the area
described here, is a loss of the dark olive pigmentation and resulting
yellowed appearance involving entire fronds and mature tissues of these
seaweeds (Figs. 34, 35).
A pattern of increased yellowing (bleaching) in
Ascophyllum is now observed, and is strongly correlated to gradients
of nutrient availability. In sheltered areas, plants growing in close
proximity to small sewage outfalls (Figs. 36 and
37) maintain olive
pigmentation while the bulk of the surrounding Ascophyllum
population yellows. On a fairly small scale, gradients of water movement
produce a similar color gradient in this seaweed, as shown in Figs.
39. Higher degrees of water movement allow Ascophyllum to maintain
its normal dark olive color year round, lesser degrees of water movement
produce summertime bleaching and wintertime darkening of color, while in
extreme shelter Ascophyllum now remains bleached in all seasons.
The yellowed, apparently nutrient-stressed,
Ascophyllum nodosum that has been long established in clean, sheltered
inlets in this region, is increasingly breaking down and decaying as a
result of environmental stress. This appears to be predominantly
wind-related desiccation, although temperature and wind patterns have
remained within normal for the region. Observed in all seasons, the
immediate effect of the extreme drying is a color change in Ascophyllum
from yellow to red in the tissue that has been killed. Subsequently the
injured tissue blackens and sloughs off, effectively cropping back these
long-lived seaweeds that may once have attained lengths of one or two
meters. For the long-time observer, a new and strikingly unusual visual
effect has been produced, of yellow seaweed beds now accentuated with
bright red, burnt-looking spots (Figs. 40,
descriptions of the life history of Ascophyllum nodosum describe
this seaweed as growing to its greatest lengths in sheltered areas, where
the risk of being dislodged by wave action (presumably the usual mode of
death?) is lowest (Lobban & Wynne 1981). The tendency of Ascophyllum
to grow best in sheltered areas is still observed here, but only up to a
point: in extreme shelter the species now appears to be dying back, and to
be doing so as a result of a lowered physical resistance, related to
nutrient stress. Sheltered intertidal rocks, which were draped with long
dark fronds of Ascophyllum in decades past, now support a
close-cropped, yellowed and wind-singed version of the seaweed (Fig.
This slow-growing seaweed appears to be experiencing a gradual net loss of
biomass by clumps that may have been established in these sheltered waters
many decades ago. There appears to be a transition happening, and the loss
of a previous level of equilibrium involving this species at these
relatively marginal locations.
Several species of Fucus (F. vesiculosis,
F. spiralis, and F. serratus) are commonly found in this
region. Fucus shares many characteristics with Ascophyllum
nodosum, including the normal olive pigmentation. An important
difference, however, lies in the habit in mature Fucus of forming
new growth and reproductive structures only at the tips of its repeatedly
branched structure. In contrast, Ascophyllum nodosum forms new
branches and reproductive growths along the length of its mature fronds.
These seaweeds are capable of internal translocation of nutrients and
products of photosynthesis towards the areas of fastest growth (Lobban &
Harrison 1994), and a significant difference in the appearance of the two
brown seaweeds now seems to arise on this basis. Because of its growth
pattern, Fucus has a natural tendency to translocate resources
towards the distal, actively growing tips, while Ascophyllum does
not. Fucus shows a similar pattern of yellowing in clean, sheltered
areas, as that described for Ascophyllum, but an interesting
reversal of the pattern of colors at the level of the organism has been
Bleaching of seaweeds is associated with a
combination of light stimulation and nutrient availability (Harvey &
McLachlan 1973). Fucus plants show a pattern of yellowing that
suggests greater light stress is experienced by the older sections of the
plant, by tissues that naturally tend to receive somewhat less light when
growing in water, since older areas are below, and partly shaded by, the
buoyant new growth. The color transition, associated with increasing
nutrient-related stress, from olive green, to yellow, to red, described in
Ascophyllum nodosum, appears in Fucus specimens too, but
tends to occur in a reversed spatial sequence. In Ascophyllum, the
least light-exposed parts of the plant tend to be the greenest, with
yellowing and reddening becoming worse towards the more sun-exposed tips
(Fig. 43). In contrast, Fucus appears to “burn” from the bottom up,
as the mature tissue is drained of nutrients to support the actively
growing tips. As shown in Fig. 45, the mature tissue of Fucus is
first to lose pigmentation, yellow, and then become prone to darkening and
disappearing, apparently ultimately due to light stress or desiccation.
This pattern of tissue loss in Fucus seems to offer contradictory
evidence to an alternate hypothesis that might be offered for the whole
suite of “bleaching” changes described in Nova Scotian seaweeds: a change
in the quality of sunlight, perhaps an increase in ultraviolet radiation.
The normal appearance of the most sun-exposed seaweed tissues, when
protected by a sufficient supply of nutrients, seems to suggest that
nutrient variability plays a major role in the observed pattern of
changes. (Also, no shifting pattern in the health or appearance of
terrestrial plants suggests that sunlight has become increasingly damaging
to plant life in this area.) The common, near-monochromatic appearance of
the two types of “brown” seaweeds at low tide (Fig. 32) has been replaced,
in sheltered areas in springtime, by a mosaic of contrasting hues: light
yellow Ascophyllum tips and dark olive Fucus tips (Fig.
Especially in sheltered locations today, the loss of
mature tissue mass in Fucus species is considerable. Rather than
growing to large sizes and ultimately being dislodged by storms, this
gradual withering seems now to be a common cause of death in these
seaweeds as they age. In an area where local residents decades ago
harvested large, bushy, live Fucus plants to fertilize their home
gardens, the seaweeds are now increasingly long, brown and stringy, with
most older tissue lost and only a relatively small amount of healthy
tissue at the tips (Figs. 47, 48,
49, 50). It is important to have such a
baseline, in a known, stable, area, to realize that a change has occurred.
The tendency toward breakdown of older tissue in the support of new growth
has undoubtedly always occurred in Fucus, but it seems to happen
now to an extreme degree. Rocks are still covered by stands of Fucus,
but the healthiest plants are tending to be smaller and younger than they
were before. The withered ‘skeletons’ of the oldest plants now
increasingly stand out in contrast to the appearance of the healthy young
growth (Figs. 51, 52). Fucus evanescens, which grows in
sewage-polluted Halifax Harbour (Fig. 6,
53), maintains deep olive
pigmentation and greater tissue integrity year round in comparison to
related species found on the clean open coast.
Although it is not universal, it is very easy to find
examples of apparently nutrient-stressed and withering Fucus (and
also yellowed Ascophyllum) that are simultaneously heavily affected
by filamentous epiphytes, another classic signal that has been associated
with eutrophication (Figs. 54, 55). The appearance of filamentous algae in
such instances therefore seems to reflect ‘pseudo-eutrophication’ rather
than true eutrophication.
Changes in kelp
Several species of kelp normally dominate much of the
shallow subtidal zone in the East Dover area, but, since these seaweeds
are less readily observed, my observations about long-term changing
patterns in kelp are made with less certainty. It seems, however, as if
the changing patterns described in Chondrus crispus and the
fucoids, essentially hold true for kelp species too. A subtle range
contraction away from the most sheltered, nutrient-poor habitat areas
seems apparent in kelp, as does a decrease in the maximum size attained by
plants, while natural breakdown associated with nutrient limitation and
environmental stress appears to be increasingly prominent.
About 10 years ago, the granite bottom contours of a
long-familiar sheltered inlet became visible for the first time (in my
40-plus years of observation) due to the disappearance of the kelp that
had previously covered the rocks (Fig. 56). The broad-bladed kelp still
grows where the cove narrows and the tidal current accelerates around the
end of the reef, but it shows no sign of recolonizing the shallow granite
bottom below the quieter water, which had long been part of its range.
Large kelp fronds similarly once obscured the underwater view of wharf
pilings in this inlet. Now the entire length and dimensions of these
pilings is easily visible, as kelp grows there today in markedly reduced
numbers and sizes. Shallow subtidal habitat with relatively low degrees of
water movement, that was covered by Fucus and kelp in the 1960s and
1970s, is increasingly dominated today by short-lived filamentous seaweeds
(Figs. 57 and 58). The disappearance of kelp beds in
Nova Scotia has been associated with increased grazing by sea urchins in
other instances (Lobban & Harrison 1994), but sea urchins vanished from
the area shown in Figs. 56, 57 and
58 at least a decade earlier than did
the kelp, and they remain absent (personal observation).
Anecdotally, beachcombers now tend to find fewer dark
brown examples (Fig. 59) and more “bleached” ones (Fig.
60), of the common
ruffled species of Laminaria. Beds of live kelp show many plants
with relatively pale pigmentation, and white rotting tips with reddened
edges (Figs. 60, 61,
62). In contrast, similar kelp growing in calm water
in well-fertilized Halifax Harbour maintains deep pigmentation throughout
the summer (Fig. 63). White rot in commercially grown kelp is associated
with nitrogen deficiency (Lobban & Harrison 1994). It is not possible to
conclude with certainty that a significant change has occurred in kelp
populations in this open coastal area. However, these few observations
offer no evidence that contradicts the hypothesis of lowered fertility
that has been suggested to explain the suite of changes observed in the
Time-series data on the nutrient content of seawater
in this region are uncommon. Trends in the seawater concentration of
nitrate may be most relevant to the seaweeds described here, since
nitrogen is generally considered to limit marine primary production.
Nitrate is naturally formed in bottom waters as a result of bacterial
breakdown of sunken organic matter. Seasonal patterns of
temperature-driven mixing of the water column raise nitrate to the surface
waters, which constitutes an important fertilizing trigger of the “spring
bloom” of phytoplankton, and is widely thought to ultimately determine the
organic productivity potential of the ecosystem (including production
resulting from “regenerated” nitrogen excreted by animals) (DFO 2003b).
Recent observations made by the Canadian Department
of Fisheries and Oceans (DFO) indicate an abrupt, unexplained, and
sustained decline in seawater nitrate inventories in Atlantic Canada.
Approximately 10 km offshore, at a location midway between Halifax Harbour
and East Dover, is “Station 2,” where the DFO monitors and records
“Nitrate concentrations in the upper water column
(0-50m) at Station 2 was (sic) similar to the long-term mean for the
central Scotian Shelf, however, concentrations in the 50-150m depth range
(bottom) were considerably lower (by 6-10uM) than normal. The reason for
the nutrient “deficit” is unclear…Nitrate inventories at Station 2 in 2001
were considerably lower in winter (by a factor of 2) than the long-term
mean levels of the central Scotian Shelf.” (DFO 2002)
A monitoring station to the north, on the
Newfoundland Shelf (Station 27), reported a similar marked decline in
nitrate, also falling abruptly in 2001, but one which persisted throughout
the year and affected both the upper and lower levels of the water column
(DFO 2003b). The declines noted in 2001 did not reverse in 2002.
Falling nitrate formation, coinciding with a rising
intensity of the spring phytoplankton bloom, presents a perplexing paradox
when an explanation is sought based on standard models of marine
production. No hypothesis, based on climate variables or other parameters,
has been offered by DFO for the reported nitrate “deficit.” Regardless,
the ultimate slowing of natural nitrate formation is consistent with the
hypothesis offered here, that seawater fertility has been falling on a
systemic scale. And declining nitrate concentrations appear to be
inconsistent with the assumption that broad changes in coastal marine
life, such as the suite of seaweed changes described here, if they have
not been caused by climate change, that they then must result from a
condition of “eutrophication.” High levels of nitrate in sewage can have a
significant negative impact on coastal ecosystems, but the declining trend
in nitrate concentrations measured at Station 2 suggests that the effects
of the sewage outflow from Halifax Harbour do not reach that far, much
less extend any further, to the East Dover area. (The population of the
city of Halifax continues to grow, and no form of sewage treatment has yet
While trends toward slowed growth and lowered
pigmentation of perennial macroalgae, along with falling seawater nitrate
levels, and widespread stunted fish growth, suggest a lowering of primary
productivity along the open Atlantic coast of Nova Scotia, simultaneous
trends towards an increasing abundance of ephemeral species of macroalgae
seem to suggest a contradictory scenario, of rising productivity, since
the latter pattern has been commonly associated with eutrophication. This
unexpected picture in Nova Scotia, of ‘pseudo-eutrophication,’ may be
related to ecological effects of a generalized loss of marine animal life.
A decline in grazer pressure on the short-lived
seaweed species may partially account for their greater accumulation of
biomass in the area described, since a major decline in the abundance of
snails, sea urchins, sea stars, large and small fish, and crustaceans, has
also been observed in this area over recent decades. Multiple species of
visible fauna, both exploited and unexploited, have experienced biomass
declines, estimated at 90% or greater, during the four decades of
observation. Declines of this magnitude have affected invertebrate species
that are major grazers of macroalgae, including periwinkles (personal
estimate of 80-90% decline over 4 decades. Once ubiquitous marine snails,
Littorina littorea, are now virtually missing from the “Littorina
zone” that was named for them (see Figs. 23 and
36). Sea urchins, once
commonly seen in this area, are now absent from near shore habitat, none
having been seen for 2 – 3 decades. It has been noted by others that:
“Reduced grazing control is apparently an important and often overlooked
factor for biomass accumulation of free-floating macroalgae under
eutrophic conditions.” (Nienhuis 1996). However, this same dynamic might
predictably lead to an enhanced accumulation of short-lived macroalgae
with high nutrient uptake rates under increasingly oligotrophic
conditions. The competitive advantage of short-lived macroalgae under
lower nutrient availability, combined with lighter grazing pressure, may
contribute to an increasing dominance of fine-structured annual seaweeds
over slower-growing, heavier perennial species should ocean fertility
fall. However, a mistaken first impression might be that the increased
mass of fine algae in a case of lowered nutrient availability has resulted
from a very different potential cause, from “eutrophication.
Grazers may play important dual roles in both
reducing the standing stock of short-lived algae and in supporting algal
growth by providing pulses of readily assimilated nitrogen (ammonium).
Invertebrate grazers, especially, may thereby provide nitrogen in excess
of that (“regenerated N”) resulting from the direct metabolism of ingested
algae, since these animals also access other food reserves, including
detritus derived from larger animals, and dissolved organic matter
(Stephens & Schinske 1961). A marked decline in invertebrate grazer
effects on the seaweed communities described here may reasonably be
assumed to have accompanied the substantial decline in their populations
that has been observed over recent decades (MacKenzie 2001, MacKenzie
A lowering of fertilizer availability to perennial
seaweeds, such as Chondrus crispus and the fucoids, may cause a
lowering of the natural ability of these plants to discourage the
accumulation of epiphytes on their tissues, since organic reserves are
needed for two of their common strategies: shedding the outer layers of
tissue, and producing repellent substances (Lobban & Harrison 1994). This
may represent another dynamic that contributes to the picture of
nutrient-starved perennial macroalgae becoming overwhelmed by a profusion
of short-lived epiphytic species, as illustrated in Figs.
Pulsed ammonium, versus a steady nitrogen content of
seawater, has been shown experimentally to enhance the ability of the
perennial seaweed, Gracilaria conferta, to resist overgrowth by
epiphytic algae (Friedlander et al. 1991). The ability of heavier
perennial seaweeds, including Fucus, Chondrus, and many kelps, to
store nutrients, and use them later to support new growth, may offer these
species a significant advantage over the faster growing, but simpler,
annuals, under a regime of intermittently pulsed fertilizer availability.
Mobile schools of many species of fish commonly inhabited these waters in
summers decades ago, and their presence has now been greatly diminished.
As providers of pulsed ammonium, even though these largely carnivorous
fish did not interact directly with the seaweeds, they may have played a
role in maintaining nutrient conditions that favoured the growth of the
relatively epiphyte-resistant, larger and more fertile, perennial seaweeds
that flourished in their presence. The sight of fish swimming in proximity
to seaweed beds, once the summertime norm found throughout this region, is
now a relative rarity.
Finally, “increasing numbers and density of filter
feeders” has been frequently reported as a change associated with
eutrophication (Schramm & Nienhius 1996). This is illustrated by the
dominance of populations of barnacles and mussels inside sheltered,
sewage-polluted, Halifax Harbour (Figs. 64,
65). Surprisingly perhaps,
even this signal may sometimes be seen to be rising in an intertidal zone
undergoing changes due to a lowering of fertility. An assessment of trends
in the “density of filter feeders” can be misleading if only small
juvenile mussels are seen
Very small mussels can feed efficiently on dissolved
organic matter (Manahan et al. 1982), an activity that places them at a
very low trophic level (with bacteria) and provides a degree of feeding
independence from immediate, new primary production. The appearance of
mussel spat alone may not signal a rise in phytoplankton production,
because they may not have developed to the point of significant reliance
on “filter feeding.” It is probably important when considering the
dominance of filter-feeding organisms as a reflection of seawater
fertility to determine patterns of growth and maturation success of those
organisms, of dynamics affecting the whole population, as well as noting
whether they are “present” or “absent” from an area. The net decadal shift
in the population of mussels in this region has been observed to be a
substantial negative one, despite their apparent occasional recent
“replacement” of stands of Chondrus crispus. The recent heavy
settlement of juvenile Mytilus edulis, as shown in Figs.
30 and 31,
has not been observed to develop into large mussels at these sites. The
few small fronds of Chondrus visible among the mussels in Fig.
are bleached, counteracting the impression of high plant nutrient loading
that might be received only by considering the fact of the presence of the
“filter feeding” young mussels. Further, rather than competing for plant
nutrients with the Chondrus (as competing annual algae species are
thought to do), the mussels, if they have any effect, should add to the
availability of plant fertilizer since they release ammonium. This
pattern, of the appearance of masses of juvenile mussels that do not
mature, might also be sometimes characteristic of the scenario of
‘pseudo-eutrophication’ that paradoxically seems to accompany falling
fertility of seawater.
The barnacle, as an immobile crustacean more fully
dependent on filter feeding than the mussel, might be a more reliable
indicator of trends in the success of “filter feeders.” A marked decline
in barnacle abundance, spanning five decades, is apparent on the open
coastline described here (MacKenzie 2001). Highly wave exposed granite
shoreline, as illustrated in Fig. 66, taken at Peggy’s Cove, N. S., which
typically supported a heavy white “belt” of barnacles above the level of
the rockweeds in the 1940’s (Stephenson & Stephenson 1972), now rarely
supports barnacle growth at this level. This declining dominance of filter
feeding intertidal animals, on the clean open coastline, suggests a trend
of lowering plankton productivity, such as would occur under a scenario of
falling ocean fertility. Regardless, trends in the distribution and range
of sizes present in any indicator organism should be assessed in addition
to noting which species are present.
Direct reflections of fertility obtained from
perennial macroalgae may prove to be the most reliable biological
indicators of seawater fertility. Objective assessments of condition
beyond color variability in seaweeds might usefully be monitored, for
example, trends in C:N ratios. However, species like Fucus, which
translocate nutrients internally, and may thereby tend to maintain a
relative constancy of C:N ratios under a shifting nutrient regime, might
be more usefully assessed on the basis of weight:length ratios, in a
manner similar to the assessment of condition in animals.
An important drawback to the use of standard
“bioindicators” of eutrophication such as the green ephemeral algae,
Ulva, Enteromorpha and Cladophora, lies in their low
specificity for the condition. Highly sensitive, these forms of macroalgae
are virtually always present in polluted waterways, but these species are
not naturally limited to living under polluted conditions. Their normal
tolerance of low, as well as high, nutrient conditions, makes the presence
of these species alone unreliable as a strong “indicator” of
eutrophication. The formation of a heavy, high intertidal belt of
barnacles in a relatively sheltered area, such as is seen in Halifax
Harbour, (Figs. 64, 65), provides a more specific bioindicator of
eutrophication because this pattern of barnacle growth is not seen in
unpolluted waters (Stephenson & Stephenson 1972). In medicine, the rarely
discovered “gold standard” diagnostic test for a disease is not only 100%
“sensitive,” like the ephemeral macroalgae for eutrophication, but is also
100% “specific,” meaning that it never shows up in cases where the problem
is absent. High “specificity” of a diagnostic indicator is important to
prevent false positive test results
Some tests or indicators help to confirm the
existence of a particular problem, while others can sometimes be used to
rule it out. An indicator that should not occur in cases of eutrophication
has been described here: an increasing tendency toward a bleaching-related
dieback of perennial seaweeds, which corresponds to those areas of habitat
providing the relatively lowest nutrient availability (usually sheltered
locations). Waters affected by eutrophication should sustain
well-fertilized seaweeds, even in shelter. Detectable only by long-term
monitoring, this may nevertheless be a valuable indicator for discerning
between cases of eutrophication and ‘pseudo-eutrophication.’
Failure to consider that both eutrophication and
falling fertility, or ‘pseudo-eutrophication,’ appear capable of inducing
many identical shifts in communities of marine organisms, including
seaweeds, may lead to confusion in the scientific diagnosis of changing
trends in coastal ecosystems. The effects of terrestrial nutrient input
are ultimately spatially limited as they are naturally counteracted by
dissipation and compensatory mechanisms in the marine ecosystem (uptake of
nutrients, sedimentation, denitrification) (Vitousek et al. 1997). The
suite of changes associated with ‘pseudo-eutrophication,’ as described
here, is strongly associated both with a decline in primary production (as
reflected in the condition of perennial seaweeds) and with a decline in
the strength of animal components of the ecosystem.
Scientific understanding of the dynamics of marine
ecosystems remains rudimentary and uncertain, and pathways that may be
linked importantly to rates of primary production remain largely
unexplored. This includes the partial dependency of mobile invertebrate
“grazers” of algae on the largest food reserve in the sea: dissolved
organic matter (DOM) (MacKenzie, 2002). There has recently been an
increasing focus in marine science on monitoring trends in the seawater
concentration of inorganic nutrients required for the growth of algae, but
no similarly organized approach to assessing the “stock” of DOM, which is
also dynamically involved in the stimulation of primary production (beyond
bacterial cycling routes). The pulsed delivery of ammonium by highly
mobile fish may also play a role that is significant, but difficult to
The loss of the net moderating effect
(grazing/fertilizing) that the formerly larger animal assemblage exerted
on the growth of marine algae may offer an explanation for the suite of
seaweed changes observed here. The pattern seems to include clear signals
of a lowering of fertility alongside changes that overlap those seen in
cases of nutrient overload; this is what I have described as ‘pseudo-eutrophication.’
Similar patterns and dynamics prevail in marine
assemblages inhabiting shoreline communities and in those of the pelagic
coastal ocean. Parallels to the patterns of change, that have been
described here in shoreline organisms, seem to exist in the adjacent
pelagic coastal ecosystem: a significant unexplained decline in the
abundance of invertebrate algae grazers (zooplankton) has accompanied a
seasonal rise in the standing stock of the ephemeral algae upon which they
graze (phytoplankton) (DFO 2000). And in this scenario, a similar dynamic,
of ‘pseudo-eutrophication,’ may underlie the trends; falling fertility may
again masquerade as rising fertility (MacKenzie 2003b).
The following trends may occur in ‘pseudo-eutrophication,’
and might be confused with similar patterns that occur in locations
affected by genuine eutrophication.
Increased standing stocks of green annual and
filamentous macroalgae (related to lowered invertebrate grazing and
animal-mediated fertilizer supply)
Declining standing stocks of perennial macroalgae
(In common with the effects of eutrophication, these seaweeds may become
heavily affected by epiphytic algae. A loss of lower depth ranges of
macroalgae may also occur under declining nutrient availability, even if
light exposure has not been compromised, due to the naturally greater
nutrient requirements of the deepest-living, shade adapted plants, which
must accumulate higher concentrations of photosynthetic pigments for
Loss of phanerogams (also associated with patterns
of stunted growth and heavy loading by epiphytes)
A trend toward episodic hypoxia of bottom water
may occur in poorly flushed coastal inlets (or at upwelling sites) due
to the tendency in ‘pseudo-eutrophication’ toward exaggerated
phytoplankton blooms in response to normal patterns of physical forcing.
The sinking and decomposition of a greater fraction of seasonal bursts
of phytoplankton primary production, coupled with an overall slowing of
oxygen generation, may contribute to oxygen depletion in the lower water
Exaggerated annual peaks in seawater
concentrations of chlorophyll a in response to normal patterns of
physical forcing of primary production (related to lowered grazing by
zooplankton in the case of ‘psuedo-eutrophicaton’)
Exaggerated summertime chlorophyll a lows
may also occur, related to the loss of the mobile animal-mediated,
pulsed supply of ammonium to the surface water. This may lead to greater
blooms of dinoflagellates and cyanobacteria, smaller phytoplankton with
a natural competitive advantage over the heavier diatoms under
nutrient-depleted conditions. These types of phytoplankton are
associated with many “harmful algae blooms,” and their increasing
prevalence may offer a parallel to the near-shore rise in filamentous
macroalgae, appearing likewise in association with both eutrophication
and pseudo-eutrophication. (These patterns may be developing on a very
broad scale: besides a global rising trend in “red tides,” a recent
analysis of two decades of satellite-derived data on global ocean
chlorophyll concentrations has demonstrated a general pattern in the
North Atlantic Ocean of exaggerated chlorophyll oscillations in response
to patterns of physical forcing. On spatial and temporal scales, decadal
trends were reported of North Atlantic Ocean chlorophyll highs peaking
at higher levels while lows fell to lower levels (Gregg & Conkright
2002). The mean annual global ocean chlorophyll change over two decades
was reported by these authors to be negative (- 6.1%), suggesting a
declining trend in overall ocean fertility.)
A surprising number of similar changes in assemblages
of marine organisms may therefore result from changing trends involving
shifts toward relative nutrient overload or toward nutrient starvation.
Direct assessments of trends in the fertility of perennial macroalgae
should help to make the differential diagnosis.
Another important distinguishing feature between
algal changes associated with animal loss, ‘pseudo-eutrophication’, and
pollution-related eutrophication, hinges on the careful assessment of
changes of populations of perennial filter feeding organisms. The
transient appearance of juvenile mussels may occur in either case.
However, mature barnacles forming a high belt in waters with low wave
action, strongly suggest genuine eutrophication, (Fig. 65), while the loss
of barnacle belts from rocky areas with high wave action suggests
‘pseudo-eutrophication’ (Fig. 66).
The explanatory hypothesis offered here, that a net
positive effect is exerted on marine primary production by the existence
of a relatively greater assemblage of active marine animals, runs counter
to standard models of marine production. The rate of new marine primary
production has classically been thought to depend on physical forcing
alone, rather than on a subtle integration of patterns of physical forcing
and animal-mediated biological forcing.
Considering the crucial ecological importance of
marine fertility, and our incomplete understanding of nutrient cycling and
the factors that regulate it, direct reflections of primary production
integrated over months or years, information potentially provided by
careful, long-term monitoring of the growth and condition of the
longest-lived autotrophs, perennial macroalgae, should be of significant
value to oceanographers. Although not a direct commercial use of seaweed
resources, this one may nevertheless ultimately prove to have important
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