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 location.

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 predominant.

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 filamentous algae.

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 crispus.

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 and 1970s.

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. 18 - Subtidal Chondrus crispus heavily overgrown with epiphytic filamentous algae.

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 periwinkle shell.

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 yellow.

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 decades ago.

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 nutrient shortage.

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 zones.

Fig. 54 - Pale Fucus in late summer, growing in very clean, clear water, is heavily overgrown by epiphytic filamentous algae.

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 pigmentation.

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 of eutrophication.

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 levels.

Decadal changes in seaweeds in Nova Scotia, Canada:
A case of ‘pseudo-eutrophication?’

by Debbie MacKenzie, April 8/2004

Email: codmother@bellaliant.net

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.

Introduction

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 have spanned.

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 ‘pseudo-eutrophication.’

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 whole.

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 seaweeds.

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 & Stephenson 1972).

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 filamentous types

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. 10 & 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. 7, 13, & 14).

Besides the rise in the abundance of green seaweeds, a multitude of filamentous species of various colors is becoming increasingly prominent (Figs. 15, 16, 17, 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 seaweed

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, & 26.

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. 30 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. 33, has 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. 38 and 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, 41, 42, 43). Classic 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. 44). 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 noted.

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. 46).

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 other seaweeds.

Nutrient availability

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 oceanographic conditions.

“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 been implemented.)

Discussion

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 2003b).

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. 18, 55, 62, and many others.

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. 31 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 quantify.

Conclusion

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 survival.)
• 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 column.
• 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 economic consequences.

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