Photosynthesis
in marine environment: An important role in controlling sea
surface temperatures
Haruka
Yoshimura, Ph.D.
Fig. 1 Conceptual diagrams: (a) temperate coastal vegetation and phytoplankton; (b) hard engineering coastal protection. (a) Photosynthetic ecosystems in marine environment heavily distribute in coastal zone: the continental shelves (0–200 meters) and the adjacent slopes. Coastal vegetation (salt marshes, mangrove forests, seagrasses, and kelp forests) provides important nurseries for marine fisheries. Marine phytoplankton, known as invisible forests (Falkowski 2002), produce approximately half of global net primary production. Supply of nutrients and organic material such as organic silicon ‘Si’ and iron ‘Fe’ compounds from terrestrial vegetation plays an essential role in the high primary productivity of coastal vegetation and active phytoplankton growth. Via CO2 sequestration, phytoplankton (e.g., Field et al. 1998; Falkowski et al. 1998) and coastal vegetation (e.g., Duarte 2017) have an important influence on global climate. When they complete their life cycle, the organic matter sinks into the deep ocean, sequentially fixed CO2 is locked over millennia. (b) Hard engineering structures such as seawalls and bulkheads destroy the most important part of marine photosynthesis. The loss of contiguous habitats between land and sea leads to deficiency of essential elements such as organic ‘Si’ and ‘Fe’ compounds for photosynthesis in marine environment. Declines marine photosynthetic production alter solar radiation balance: Increased evaporation and increased fraction of heat (sensible heat and longwave radiation). The alteration of surface energy balance accelerates negative impacts of climate change. |
1. Introduction
Landscape
architecture and management for coastal ecosystem
functions. Photosynthesis in marine environment
is a biological process of global importance, having an
influence on climate and providing a basis for resilience of fisheries.
In historical Eastern philosophy,
management of marine resources was considered as a core issue of governance for
food security to supply affordable and high-quality animal protein for people. Japanese
land governance in coastal zones was unique in translating learning-based
knowledge into effective policy and management
strategies.
At
the beginning of the 21st century, photosynthesis in marine environment has degraded,
causing adverse effects in climate change and losing resilient fisheries. Edo,
estimated population of over 1,000,000 as early as the middle of the eighteenth
century (Sansom 1963; Uspensky 2003), is a success case in land governance and
coherent national coastal strategy.
Ancient
Japanese architects and decision-makers were aware that cool, clean and clear
seawaters are essential for abundant fisheries resources, through the learning-based
approach over millenniums via dialogue with dynamic earth-surface system. For
marine ecosystems restoration, the unique learning-based approach in Eastern
philosophy is applicable for planning/management of coastal zones around the
world. Scientific translation of the historical Eastern
philosophy facilitates the application in land-use planning/management.
Photosynthesis
in marine environment.
All life in
earth, including human beings, stems primarily from the conversion of solar
radiation energy by photosynthesis into biochemical
energy. Photosynthesis
plays a major role in conversion of the inorganic carbon in atmosphere (carbon
dioxide, CO2) into organic matter—the
sugars, amino acids and other biological molecules. In marine environment, photosynthetically
active solar radiation (400 to 700nm) or sunlight penetrates with a maximum depth of 200 meters based on the light absorption
properties of salt water. Therefore, marine ecosystems that contribute the conversion of CO2 into organic matter, also known
as primary production, heavily distribute the zones from the coastlines
to a depth of 200m of continental shelves (Fig. 1). Marine photosynthetic
organisms use the dissolved CO2 in the ocean to produce organic
matter.
Most of earth—70.8%, or 362 million square kilometers—is covered by oceans and major seas. The continental shelves (0–200 meters) and adjacent slopes, that covers less than 10% of the world ocean (32 million km2), yield 90% of marine fisheries annually (Garibaldi and Limongelli 2002; Pauly et al. 2002). In contrast, the open ocean is often referred as ‘the blue desert’ owing to low primary production. Large pelagic fishes such as tunas migrate over the long distances that separate isolated food patches.
2. Declining
marine photosynthetic production (conversion of CO2 into organic
matter)
Vegetation in
sea-land interface
Salt marshes. Salt marshes
and their associated networks of drainage channels and embankments are major
coastal habitats in temperate zones. Salt marshes occur the transition zones
between land and sea where are subject to extreme daily and seasonal changes of
water levels and salinity, while they are one of the most productive ecosystems
(Odum 1971; Whittaker and Likens 1973).
Human
society has frequently classified coastal wetlands as ‘worthless’ areas. Over
time, coastal wetlands have been drained and filled to provide space for
agriculture, and building/industrial sites. Approximately, 50% of the original
salt marshes have been degraded or lost globally (Barbier et al. 2011). In some areas in US, Canada, Europe and Australia, 67% of the
original wetland vegetation of estuarine and coastal seas was lost (Lotze et
al. 2006).
Mangrove
forests. On tropical and sub-tropical
coastlines, the sea-land interface is covered mangrove forests. The dense thickets of mangroves create
shallow water swamps that extend along estuaries and/or along coastlines. The
tree foliage of thick leaves shields intense solar radiation and limits
temperature extremes, and interconnecting aerial roots (roots above ground)
systems attenuate wave energy. Accordingly, the mangrove swamps provide
important nurseries for marine fisheries (Moyle and Cech 2004).
Mangroves are
highly productive ecosystems with net primary production (difference between autotrophic photosynthesis and respiration)
equivalent to that of tropical humid evergreen forests.
Mangroves that thrive in soft sediments have been evolved unique forms in CO2 sequestration; Mangroves allocate much more fixed carbon
into soil than tropical humid evergreen forests (Alongi
2014).
Total area of mangrove habitats along the shorelines
of the world is estimated roughly 1.7 × 10 km2
(Valiela et al. 2001). Mangroves occupy 0.5% of total global coastal area
but account for approximately 10–15% of total CO2 sequestration in the coastal ocean (Alongi
2014). At least 35% of the original mangrove forests has been lost since the
early 1980s, due to human activities such as aquaculture mainly shrimp farming,
wood exploitation for industrial-level lumber and wood-chip production, and
industrial/urban development (Valiela et al. 2001).
Although rates of mangrove deforestation have
decreased (Friess et al. 2019), mangrove habitats are regressing and
fragmenting globally (Carugati et al. 2018; Bryan-Brown et al. 2020).
Seagrasses.
Seagrasses are flowering plants (angiosperms), which form seagrass meadows in
shallow seas on all continents except Antarctica. In temperate zones, seagrass
meadows distribute from the intertidal to about 60m (200ft) depth in clear
waters. The dominant species in temperate regions is eelgrass (Zostera
marina) that adapts to thrive better in cooler waters (Unsworth et al. 2015).
Seagrass meadows are among the most productive plant communities, comparable to
intensively cultivated crops (Duarte and Chiscano 1999). Owing
to the provision of nursery and foraging grounds for invertebrates and fish, seagrass
meadows support major fishery productivity such as Alaska (Walleye) Pollock
(介宗鱈, Theragra
chalcogramma), Atlantic Cod (Gadus morhua), Pacific Cod (真鱈,
Gadus macrocephalus), Atlantic Herring (Clupea harengus), and Pacific
Herring (鰊, Clupea pallasii) (Unsworth
et al. 2018).
In
tropical regions the dominant species is turtle grass (Thalassia testudinum),
which distributes often associated with coral reefs and mangroves.
Historically, seagrass meadows provided forage and habitat for enormous numbers
of sirenians (dugong and manatee) and sea turtles, as well as commercially
important fish species (Jackson et al. 2001).
Seagrass
meadows are lost globally at fast rates. At least
one third of the area has been lost since World War Ⅱ (Orth
et al. 2006; Waycottet al. 2009). In some temperate
sites in US, Canada, Europe, and Australia, 65% of the original seagrasses was
lost (Lotze et al. 2006).
Kelp forests. Kelp forests—undersea
forests of brown alae (order Laminariales)—form unique habitats in coastal
regions of temperate and Arctic areas worldwide. In temperate waters, they are
typically found 6m (20ft) and 30m (98ft). The kelps are anchored to rocky or
sandy bottoms with holdfasts (not roots), and have long fronds (resembling to
true leaves) extending to the surface. The fronds of a species of kelps (Saccharina
angustata, an edible kelp highly flavorsome for Japanese cuisine,
occurs in northern Japan) grow up to 20m (66ft). The complicated canopy
structure of the kelp forests provides a variety of habitats for invertebrates
and fishes (Moyle and Cech 2004). Kelp forests have
high rates of primary production. The net primary production (the difference
between the amount of photosynthetically produced organic matter and
respiration) is comparable to a tropical rain forest (Mann 1973).
In
some temperate sites in US, Canada, Europe, and Australia, 48% of the original kelp
forests was lost (Lotze et al. 2006). The kelps grow best cold waters.
Therefore, increased ocean temperatures, together with cumulative effects of other
stressors, reduce their growth, consequently have resulted in collapse of kelp
forests along many temperate coasts globally (Filbee-Dexter and Wernberg 2018).
Ocean’s
invisible forests: marine phytoplankton.
Phytoplankton constitute the basis of marine food
webs. Each year, marine phytoplankton generate approximately
half of global net primary production (the net mount
of photosynthetically fixed carbon minus the organic matter used up in
respiration) (Field et al. 1998; Falkowski 2002).
They proliferate quickly, increasing in number by many orders of magnitude in
just a few days. Despite accounting for only 0.2% of global producer biomass,
marine phytoplankton attain such high net primary production by its rapid life
cycle (Field et al. 1998; Falkowski
2002).
Tiny
single-celled algae, “diatoms, dinoflagellates, and
haptophytes,” are dominants of photosynthetic producers in continental shelves
and seasonal blooms in temperate waters (Simon et al. 2009). The diatoms, with
an estimated 200,000 different species ranging in size from a few
micrometers to a few millimeters, are the most essential group of
eukaryotic phytoplankton. They have been estimated to contribute about 40% of
marine primary productivity (Tréguer et al. 2018). Diatoms
generate most of the organic matter that serve as food for life in the sea:
diatoms are consumed by zooplankton (small crustaceans such as copepods
and krill; larva of fish, squid, lobsters and crabs). Sequentially, these
smaller herbivorous zooplankton provide food for larger zooplankters and for forage
fish: small, schooling, filter-feeding fish such as herring, sardines, and
anchovies. The forage fish are then consumed by larger predators including diverse
fish species of commercial importance (Fig. 2). In coastal waters, diatoms
support the productive fisheries. They produce most of the organic matter
consumed rapidly by zooplankton and serve as a base for marine food webs (Armbrust
2009).
Marine
phytoplankton have declined in the world’s oceans by
about 40% since 1950, possibly in response to increasing
sea surface temperatures (Boyce et al. 2010,
2014). Higher ocean temperatures inhibit normal
metabolism and lower productivity of marine phytoplankton (Toseland et al. 2013).
Fig. 2 Schematic representation: (a)
example food web sustaining resilient fisheries; (b)
example of collapse of trophic transfer in marine food web. (a) Phytoplankton constitute the basis of marine food webs, providing resilience for
fisheries (e.g., Pauly and Christensen 1995). (b)
Rising water temperatures along with nutrient pollution fundamentally alter
structure of primary production, known as ‘harmful
algae blooms.’ Changes in the species composition of primary production,
in turn, degrade the food webs. For instance, bloom of dinoflagellate green Noctiluca in tropical waters causes modification
of trophic transfer in food webs and leads to collapse of fisheries (do Rosário
Gomes et al. 2014; Goes et al. 2020).
The most important zooplankton such as copepods and krill do not feed on green Noctiluca, while salpas and jellyfish
proliferate consuming it. |
3.
3. Marine photosynthesis: influence on climate
3.1 Structure
and function of marine photosynthesis in solar radiation balance
In
terrestrial biosphere, leaf canopy structure, photosynthesis and transpiration dissipate solar
radiation energy and control
temperature (http://harukanoor4.blogspot.com/2019/).
Plant pigments absorb the
visible range of solar radiation. Subsequently, most of the absorbed energy is used in
biochemical pathways of photosynthesis (Blackburn 2007). On land, stratified canopy foliage of vegetation shields
solar radiation, keeping soil and soil moisture cool. Deep and extensive root systems
uptake cool moisture from the soil and extract cold groundwater, and
accordingly cool moisture is releasing via transpiration.
In marine environment, vegetation
structure and photosynthesis dissipate solar radiation energy without a large increase in
temperature. The vegetated coastal habitats and phytoplankton absorb solar radiation energy and control
temperature. As mechanisms of photosynthesis
on land and in the oceans are essentially similar, absorbed
solar radiation energy by the photosynthetic pigments of coastal vegetation and
phytoplankton is used in biochemical pathways of photosynthesis.
By the floating canopies of seagrass meadows consist
of long green leaves over 1.0m (39.4in) and of kelp forests consist of long
ribbon-like fronds, submerged coastal vegetation shields solar
radiation and controls temperatures
suitable for their growth. Free-floating phytoplankton, distribute three quarters of
the earth’s surface, shield solar radiation (like a cloud in the
sky) and moderate temperatures over vast extent of oceans.
3.2 Photosynthesis
in marine environment:
A role of global CO2 sequestration
Marine
phytoplankton’s primary
production (conversion of CO2 into organic matter) has an influence on global climate via CO2
sequestration (Field et al. 1998; Falkowski et
al. 1998; Falkowski 2002). When marine phytoplankton
complete their life cycle, the organic matter sinks from the surface layer into
the deep ocean before it decays. The organic matter released below about 200m
is locked over millennia, because the colder temperature—and higher density—of this water prevents it from
mixing with the warmer waters above (Falkowski 2002). In this process, known as
the biological pump, diatoms play a key role, because diatoms’ silica shells
provide ballast in transporting carbon to the deep ocean (Tréguer et al. 2017).
Similarly, primary production of vegetated
coastal habitats (salt
marshes, mangrove forests, seagrasses, macroalgal beds) has an influence
on global climate via CO2 sequestration.
The vegetated coastal habitats produce organic carbon far in excess of local
requirements, subsequently a large surplus of organic carbon (about 40% of
their net primary production) sink as sediments in the continental shelf or the
deep ocean, providing a function of CO2 sequestration. Despite
occupying only 0.2% of the ocean area, coastal angiosperms (flowering plants)
dominated ecosystems contribute approximately half of the total CO2 sequestration in the ocean (Duarte et al. 2005; Duarte 2017).
Through the biological pump, phytoplankton and coastal
vegetation remove CO2 from the surface waters and atmosphere and store it
in the deep ocean. However, the capacity of CO2 sequestration in the deep sea is
rapidly weakening by the declining
phytoplankton and vegetated coastal habitats.
3.3
Declines of marine
photosynthesis cause
increase in sea surface temperatures
Decline
of marine photosynthesis (coastal vegetation and
phytoplankton) alters solar radiation balance (Fig. 1). The decline
of marine photosynthesis leads to decrease of absorbed solar radiation
energy by photosynthetic
pigments. The fraction
of solar radiation energy previously absorbed by photosynthetic pigments is absorbed sea water. Loss of shield-effect of
biological structure in marine environment increases absorbed solar radiation
energy by sea water. These factors possibly result in increase in sea surface
temperatures.
Marine heatwaves—ocean
areas of extreme high sea surface temperatures that
persist for days to months—have increased sharply in all major ocean basins
over the recent decade (Frölicher and Laufkötter 2018; Oliver
et al. 2018; Smale et al. 2019). The longer and
more frequent marine heatwaves (Oliver et al. 2018)
are already impacting marine ecosystems: the submerged aquatic vegetation,
seagrass meadows and kelp forests, has been lost (Smale et al. 2019).
Marine phytoplankton (mostly
diatoms), that sustain the marine food webs, thrive
better in cooler waters. As higher ocean temperatures significantly affect metabolism
and lower productivity of phytoplankton (Toseland et al. 2013), the extreme
high sea surface temperatures negatively affect phytoplankton productivity. If phytoplankton
are lost by these extreme temperatures, the marine
food webs could collapse.
3.4
Rising sea surface temperature: influence in weather and climate
The marine heatwaves induce photosynthesis decline. Which in turn causes additional increase in sea surface temperatures, as the fraction
of solar radiation energy that was once absorbed by photosynthetic pigments is
absorbed by sea water.
Warmer sea surface temperatures could increase the
frequency and severity of tropical cyclones (Trenberth 2005; Hoyos et al. 2006;
Kerr 2006).
Evaporation from the oceans can increase, as the fraction
of solar radiation energy that was previously absorbed by photosynthetic
pigments and used photosynthesis processes is allocated
to latent heat flux (solar radiation energy used to evaporate water from
the ocean surface). Due to moisture source of precipitation supplied by the
warmer wetter marine air, increased evaporation from the oceans may cause
changes in precipitation pattern: torrential rainfalls by
frontal systems and/or tropical cyclones, and heavy snows by squall lines
along cold fronts, which occur occasionally and irregularly.
4. Rising
sea surface temperatures degrade resilience of marine ecosystems: Harmful algal
blooms
Rising water
temperatures along with nutrient pollution (e.g., Anderson et al. 2008;
Heisler et al. 2008) fundamentally alter the phytoplankton community structure
in various ways. Harmful algal blooms have a
negative impact on marine ecosystems and coastal fisheries worldwide. Among the
5,000 species of marine phytoplankton, some 300 species produce blooms with
water discoloration (known as ‘red tides’), while 80 or so species have the
capacity to produce potent toxins (Hallegraeff 2003).
Dinoflagellate genus
Alexandrium.
The dinoflagellate genus Alexandrium is a
globally distributed harmful algal genus with many species and strains that are
known to produce paralytic shellfish toxins, known as saxitoxins. The impacts of paralytic
shellfish toxins include human intoxications and death through the marine
food webs: filter-feeding bivalves, such as mussels,
cockles, oysters and scallops consume the dinoflagellates, transferring them
from the gills to digestive organs where the toxins concentrated. The
concentrated toxins are passed to higher trophic levels of the food webs. The incidence
of human paralytic shellfish toxins poisoning could occur by the consumption of
the contaminated shellfish or fish (Anderson et al. 2008,
2012). Saxitoxins are also produced by dinoflagellate genus Gymnodinium
and Pyrodinium, as well as several genera of predominantly freshwater
cyanobacteria (e.g., Anderson et al. 2012).
Dinoflagellate
genus Karenia. Florida red
tides are predominantly associated with the blooms of the
toxic dinoflagellates Karenia brevis (Fleming
et al. 2011). This dinoflagellate produces a suite of potent natural neurotoxins,
called brevetoxins. Brevetoxins are neurotoxins that interfere with
proper nerve transmission, which in turn affects the central nervous system and
induces immune depression. Human intoxication from neurotoxic shellfish
poisoning is caused by consuming contaminated shellfish, because filter-feeding
shellfish accumulate the neurotoxins. The brevetoxins are tasteless, odorless,
and heat and acid stable, and cannot be removed by food preparation (e.g.,
cooking contaminated seafood).
Due to relatively fragile unarmed cell structure, the Karenia brevis organism is easily broken open by
in wave action along beaches, releasing the toxins. Inhalation of the aerosol
of contaminated salt spray containing the toxins and organism fragments is
causing respiratory irritation to humans and mammals. Symptoms
in humans of exposure include stinging eyes and nose, dry choking cough and
onset of asthmatic attack (Pierce and Henry 2008; Fleming et al. 2011).
The toxins cause severe impacts on natural resources: mass mortalities of
fish, marine mammals, sea turtles and sea birds (e.g., NOAA 2021). Although Florida
red tide blooms have been documented since the 1840s, these and other red tides
appear to be increasing in incidence, duration and geographic spread. The brevetoxin-producing
Karenia brevis is found throughout the world’s ocean, including New
Zealand (Nozawa et al. 2003) and Mediterranean Sea (Tsikoti and Genitsaris
2021).
The other toxin-producing blooms in the genus, Karenia,
have been identified in diverse geographic locations worldwide. Karenia selliformis is responsible for the
production of the toxins gymnodimines that block
nicotine acetylcholine receptor in our human nerve system. The toxins gymnodimines along with the hemolytic
capability, the blooms of K. selliformis are causing
mass mortalities of a variety of coastal wildlife (Tatters et al. 2010). The blooms of K. selliformis have been
reported from coastal waters of New Zealand, Mexico, Tunisia, Kuwait, Iran,
China and Chile (Mardones et al. 2020).
Karenia mikimotoi is a bloom-forming toxic dinoflagellate. In Japan, blooms
of K. mikimotoi caused mass mortality of
pearl oyster (Pinctada fucata) have been documented since the 1930s, and
these blooms appear to be increasing in incidence, duration and geographic
spread (Go et al. 2016). Blooms of K. mikimotoi
have been reported widely in subarctic (Scottish waters around 60°N, Davidson et al. 2009), temperate (e.g.,
Qinhuangdao in China around 40°N, Chen et al. 2021;
the Aegean Sea around 40°N, Tsikoti and Genitsaris 2021) to sub-tropical
(Zhanjiang in China around 21°N, Chen et al. 2021) coastal waters. The production of reactive oxygen
species by the dinoflagellate (Li et al. 2019) leads
to mass mortalities: Most of marine faunas use gills as respiratory organ to extract
dissolved oxygen from water and to excrete carbon dioxide. The gills are
oxidative damaged by the reactive oxygen species (e. g., Kim et al. 1999, López-Cortés
et al. 2019 in dinoflagellate Margalefidinium polykrikoides). Due to the
toxic effect of reactive oxygen species along with the hemolytic and cytotoxic
capability of K. mikimotoi (Li et al. 2019), blooms
of K. mikimotoi resulted in extensive
mortalities of marine organisms: benthic organisms including annelids and
molluscs and some species of fish (Davidson et al. 2009);
filter-feeding bivalves such as clam (Ruditapes philippinarum), oyster (Crassostrea
gigas) and scallop (Mimachlamys nobilis) (Go et al. 2016).
In autumn 2021, blooms of K. selliformis in association with K.
mikimotoi in Hokkaido Island in northern Japan (around 43°N) killed nearly
30,000 salmons (Oncorhynchus keta and O. masou) and resulted in
extensive mortalities of benthic organisms including commercially important sea
urchin (Strongylocentrotus intermedius) and sea cucumber, caused a
catastrophic damage to the local fisheries (Hokkaido
government Japan, 2021).
Dinoflagellate Noctiluca
scintillans. The globally distributed dinoflagellate Noctiluca
scintillans (quite large, 0.2–2mm, typically around 0.5mm) is one of most important and abundant red
tide organisms. It is known that bioluminescent Noctiluca scintillans occurs
in two forms. Red Noctiluca acts as a microzooplankton grazer in the
marine food webs, which occurs widely in temperate to sub-tropical coastal waters.
The other form of green Noctiluca can survive
without an external food supply owing to source of photosynthetic products from
symbiont Pedinomonas noctilucae inside the cell. Though it also
feeds on other plankton, protozoans, detritus, and fish eggs, when the food
supply is abundant. Green Noctiluca occurs mainly in tropical waters (Turkoglu
2013). The photosynthetic symbionts in the cells of green Noctiluca have
higher carbon fixation capability than trophically
important diatoms at lower oxygen concentrations (do Rosário Gomes et al.
2014). In the tropical oceans, zones of low oxygen concentrations
have expanded since the 1960s (Stramma et al. 2008) due to nutrient loading
from synthetic fertilizers in agriculture and from treated/untreated sewage
effluent. As the dinoflagellate green Noctiluca can
thrive under hypoxic conditions (do Rosário Gomes et al.
2014), low oxygen concentrations of seawaters give green Noctiluca a
competitive advantage, suppressing diatoms.
Green
Noctiluca. Blooms of green Noctiluca were first observed in the open ocean
waters of the Arabian Sea in the early 2000s, have
occurred every year during the winter monsoon, from January to March (do
Rosário Gomes et al. 2014; Goes et al. 2020).
Although Noctiluca blooms are non-toxic, they can cause massive fish and
marine invertebrates kills. The cells of Noctiluca accumulate toxic
levels of ammonia, which is excreted into surrounding waters. The ammonification
of seawater and excavating oxygen deficiency have caused the severe mortality
of fish and marine invertebrates.
Winter phytoplankton blooms that previously comprised mainly diatoms have
been replaced by widespread blooms of green Noctiluca.
Diatoms dominant blooms provide basis for marine biodiversity, sustaining resilience
of fisheries: diatoms feed a wide range of primary
consumers (copepods, krill, shrimp, forage fish), which in turn are consumed
by higher trophic levels of predators including diverse fish species of commercial
importance (Fig. 2, a).
Green Noctiluca are largely unpalatable and they
are not consumed by most of zooplankton (small crustaceans such as
copepods and krill; larva of fish, squid, lobsters and crabs), except salps
(small, gelatinous, filter-feeding tunicate) and jellyfish (Goes et al. 2020). The abundance of green Noctiluca causes low
abundance of other zooplankton, which in turn has led to reduction of food
availability to higher trophic levels of predators including
diverse fish species of commercial importance. Thus, collapse of the
traditional diatom-sustained food webs causes decline of
fisheries
(Fig. 2, b).
Fisheries plays an important role as the primary source of protein and
income for a coastal population of nearly 120 million people in the countries
of the coast of the Arabian Sea, India, Pakistan, Somalia,
Yemen, and Oman. The collapse of marine food web and
resulting loss of fishery resources has the potential to exacerbate
socio-economic turmoil in countries like Somalia and Yemen where are currently
being challenged by unrest, poverty, and deprivation (do Rosário Gomes et al.
2014; Goes et al. 2020).
Red Noctiluca. Red Noctiluca is one of the most common red tide forming
organisms. Blooms of red Noctiluca, occur frequently in temperate to subtropical coastal waters, are
considered benign. However, red Noctiluca blooms may lead to collapse of
marine food webs and consequent loss of fishery resources. Red Noctiluca
does not support food webs, because they are not consumed by most of
zooplankton except salps and jellyfish. Batistić et al. (2019) suggest that blooms
of Noctiluca and resulting salp blooms alter marine food webs by the reduction of food availability to primary
consumers and consequential decrease of higher trophic levels of predators, in a
case of the temperate sea of the southern Adriatic. Thus, common red tides of Noctiluca
may have caused decline of fisheries in temperate to subtropical regions in the
world.
Pennate
diatom genus Pseudo-nitzschia. Diatoms
represent one of the most important groups within marine phytoplankton, forming
the base of the food web in many marine ecosystems. Most diatoms are
considered benign,
but some are known to cause harm by the production of a phycotoxin. Several
species of the pennate diatom belong to the genus Pseudo-nitzschia
are known to produce the neurotoxin domoic acid.
A toxic bloom of Pseudo-nitzschia occurred in 1987 in the estuaries of
Cardigan Bay, eastern Prince Edward Island, Canada, and led to an outbreak of
human poisoning due to consumption of contaminated mussels: at least 107
illness and killed at least 3 elderly people. Symptoms included abdominal
cramps, vomiting, and neurologic responses involving disorientation and memory
loss. Due to the neurological disorder, this human
poisoning is known as amnesic shellfish poisoning (Bates
et al. 1998).
Domoic acid interferes
neurotransmission in glutamate receptors,
subsequently causes damage and death of nerve cells of glutamate receptors.
These receptors are widely distributed in the hippocampus (associated with
memory retention) in human brain, hence domoic acid poisoning induces the
memory loss (Bates et al. 1998).
Blooms dominated by toxic Pseudo-nitzschia are increasing in frequency and
duration along most of the world’s coasts: United States, Canada, Mexico, South
America (Chile, Argentina, Uruguay, and Brazil), Australia, New Zealand, Africa
(South Africa, Namibia, Tunisia, and Morocco), Europe (UK, Ireland, France,
Denmark, Portugal, and Spain), also in upwelling regions of open oceans (where
deep, cold, nutrient-rich water rises toward the surface) (Trainer et al. 2012).
The trophic transfer of domoic acid has led to dramatic mortality events
of marine mammals and birds. For instance, over 400 sea lions died and many
others displayed signs of neurological dysfunctions along the central
California coasts linked to a toxic Pseudo-nitzschia bloom in 1998
(Scholin et al. 2000).
Toxic Pseudo-nitzschia cells are consumed by sardines and
anchovies, subsequently the neurotoxin domoic acid transfers higher levels of
the marine food webs. Meanwhile, the toxin-containing diatom cells during
senescence transport downward rapidly and reach the benthos, as the siliceous
cell walls of diatoms act as ballasting material. The toxin in bottom sediments
persists long in colder deeper waters in dark conditions and be readily
available for bioaccumulation. Resulted high level of domoic
acid in benthic organisms (e.g., crabs; spiny oyster; flatfish;
cephalopods; filter-feeding bivalves such as mussels, scallops, calms)
adversely affects marine ecosystems (Sekula-Wood et al. 2009). Which, in turn
lead to economically disruptive fishery closure required to protect human health
(Trainer et al. 2012; Ryan et al. 2017).
‘Brown
tides’ picoplankton Aureococcus anophagefferens. ‘Brown tides’ caused by the harmful picoplankton (0.2–2 µm) Aureococcus
anophagefferens had never been documented before 1985 but have recurred in
shallow bays/estuaries in the United States and South Africa since that time (Bricelj
and Lonsdale 1997; Gobler et al. 2011). Brown tides of Aureococcus
anophagefferens occurred in 2009 in the north-western Bohai Sea, China, and
have recurred since then (Zhang et al. 2012; Huang et al. 2020).
Brown tides have caused inhibitory
effects on growth in suspension-feeding bivalves such as hard clams, mussels
and bay scallops throughout their larval development (Bricelj and MacQuarrie
2007). Recent research shows that the brown tide alga Aureococcus
anophagefferens produces a potent toxin of hemolytic and cytotoxic effects
(Huang et al. 2020). Due to severe mortalities in wild and cultured bivalves,
brown tides have caused collapses of the shellfish industry.
The brown tides result in marine food web collapses. Under the
progressive changes by urban runoff in coastal seawaters: increasing water
turbidity and organic matter, the brown tide alga Aureococcus anophagefferens
outcompetes other useful phytoplankton as primary producer such as diatoms. By
the loss of the base for marine food webs, energy flow from the first trophic
level (diatoms) to higher trophic levels does not occur.
In addition, severe light attenuation due to brown tides led to massive
loss of eelgrass meadows (Bricelj and Lonsdale 1997). These loss of eelgrass
meadows serving as important spawning and nursery grounds for shellfish and
fishes has had indirect impact on fisheries. Brown tides alter the once
productive shallow bays/estuaries to the seas of ecological degradation.
Broad geographic distribution of brown tide alga Aureococcus
anophagefferens has been identified in USA, from Maine to Florida (Bricelj
and MacQuarrie 2007). In anthropogenically modified bays/estuaries, conditions
of increasing water turbidity and organic matter that promote the harmful agal
proliferation have become prevalent, suggesting a potential risk of further
expansion of brown tides (Gobler et al. 2011).
Cyanobacteria.
Cyanobacteria (in the size 0.2–2
µm) are oxygen-producing bacteria (not algae) that use sunlight to
convert CO2 into
biomass. Cyanobacteria generally grow better higher temperatures (often above
25℃) than do other phytoplankton such
as diatoms (Paerl and Huisman 2008). Consequently, cyanobacterial
blooms in freshwater
and marine environments are currently increasing globally owing to rising
temperatures coupled with nutrient loading from urban, industrial and
agricultural sources (Huisman et al. 2018).
Bloom-forming
cyanobacteria produce
a variety of cyanotoxins damaging liver, digestive and neurological systems of
birds, mammals and humans (Carmichael and Boyer 2016; Huisman et al. 2018). In
terms of global hydrological cycle, fresh water contributes only 2.5% of the
total volume of water in Earth. Only a tiny proportion (0.296%) of the world’s
fresh water is present as surface water (water reserves in lakes: 0.26%; swamp
water: 0.03%; river flows: 0.006%) (Shiklomanov 1993). Cyanobacterial
blooms in freshwater, including Lake Victoria in Africa, Lake Erie in North
America, Lake Taihu (太湖) in China, and Lake Biwa (琵琶湖) in Japan (Ishikawa et al. 2002), are a growing concern for our drinking
water that rely on surface water.
The North American Great Lakes are a vital
freshwater resource, containing roughly 20% of the Earth’s available surface
freshwater. Cyanobacterial blooms have recurred annually since the late 1990s’
in some of the most populated areas of the Lakes (Steffen et al. 2014). In
early August 2014, a ‘do not drink’ advisory was issued for Toledo, Ohio, USA, due
to high concentrations of microcystins (potent liver toxins produced by a variety of
cyanobacteria), which resulted in over 400,000 residential customers and
hundreds of businesses being without tap water for nearly 48 hours (Huisman et al. 2018). Microcystins, potential carcinogen, are stable in water, and boiling
does not remove or destroy these toxins (Falconer and Humpage 2005).
Cyanobacterial blooms are also expanding in estuarine and marine ecosystems throughout the
world, including the Baltic Sea in Europe (Stal et al. 2003; Kahru et al. 2020),
the Mediterranean Sea (Spatharis et al. 2012), and Florida bay in USA (Butler
et al. 1995; Glibert et al. 2009). The microcystins are produced by cyanobacterial blooms in the enclosed Isahaya Bay in
southern Japan by dyke defense structure against coastal floods (7km or 4.4mi long,
constructed in 1997) (Takahashi et al. 2014). Owing to cyanobacteria’s intracellular
gas vesicles acting as flotation devices, cyanobacteria float upward and
accumulate in dense surface blooms with a wide array of colors, various shades
of green, red, brown, yellow and pink. These surface blooms increase light
attenuation, and have been implicated in the massive loss of seagrass meadows (Butler et al. 1995; Glibert et al. 2009). Decreased light
penetration suppresses the essential phytoplankton that serve as a base for marine
food webs through competition for light (Paerl and Huisman 2008).
Die-off of blooms may deplete oxygen. Consequent
hypoxia (having too little oxygen) causes the death of fish and benthic
invertebrates (Diaz and Rosenberg 2008; Huisman et al. 2018). Cyanobacteria
thrive well under hypoxic conditions, as they originated around 3 billion years
ago in the absence of oxygen in the ocean-atmosphere system of the early Earth
(Schirrmeister et al. 2015).
5.
Photosynthesis
in marine environment supported
by land-sea interactions
Marine
productivity needs essential elements supply from land. Organic matter dynamics by land-sea interactions play an essential role in nutrient supply to marine
primary productivity to support bodily structure (such
as organic
silicon ‘Si’ compounds) and metabolism (such as organic iron ‘Fe’ compounds).
Terrigenous input of nutrients and organic material
makes an important contribution in estuarine and coastal productivity. For
instance, the highly productive coastal Mediterranean fishery off the Nile
River delta collapsed after the construction of the Aswan Dam, due to decreased
nutrients in the floodwater that supported large diatom blooms and a productive
fishery, particularly for sardines (Milliman 1997).
Diatoms, the
most essential group of marine phytoplankton, are unique because of their cell
walls made of silica, and the growth rates are limited
by the supply of silicate (Smetacek 1998). Dam construction in the Danube River is a notable case. Decreased
dissolved silica discharge to the Black Sea due to the dam crosses the Danube
River has led to a shift in the composition of phytoplankton species form diatoms
(siliceous) to non-siliceous such as dinoflagellates. The observed changes in
Black Sea surface waters strongly suggest that materials form the terrestrial
environment such as silica support the food web structure in coastal seas (Humborg
et al. 1997; Milliman 1997).
Many plants, particularly grasses (Poaceae) including common reed (Phragmites australis,
found riparian zones and wetlands throughout temperate and tropical regions of
the world), Equisetaceae (horsetail family) and Cyperaceae (family of graminoid)
are rich in silica as structural materials (Currie and
Perry 2007). Rivers are the main transporters of silica from the
terrestrial environment to the oceans (Smetacek 1998). Supply of silica derived
from terrestrial vegetation may play an essential role in primary productivity
in the coastal and marine environments (Conley 2002).
In many ocean realms, iron (Fe) deficiency is
limiting phytoplankton production (Martin and Fitzwater 1988). The growth rates
of marine phytoplankton are restricted by the availability of soluble Fe
(e.g., Kuma and Matsunaga 1995).
Matsunaga et al. (1999) indicate that the macroalgae
growth is also restricted by the availability of soluble Fe, which derives from
humic substances of forests via the decomposition of leaf litter.
All living things are made of one or more cells, and
all the cells are mostly composed the same substances that carry out similar
life functions. Cytochromes, a group of hemoprotein cell protein with a central
Fe atom at its core, serve a vital function in both photosynthesis and cellular
respiration. As cytochromes are found all animals and plants, and many
microorganisms, humus and organic matter from terrestrial vegetation (e.g.,
leaf litter, wood, and other plant parts) that falls into rivers and coastal
seas contains cytochromes. Hence, soluble Fe and/or cytochromes derived from an
enormous amount of organic matter from terrestrial primary productivity may
contribute marine primary production such as phytoplankton and macroalgae.
Coastal forests
as critical juncture. Coastal zone plays a significant role in Fe supply pathway of land-sea
connectivity. In the second half of the twentieth
century, Hokkaido Island in northern Japan has experienced a collapse of
fisheries coincide with decline of kelp forests, which occurred concurrent with
massive deforestation of old-growth boreal forests. Until 1960s, Hokkaido
Island was covered with old-growth boreal forests, dominated by conifers (e.g.,
spruce, Picea jezoensis, up to 40m; fir, Abies sachalinensis, up
to 35m), mixed with deciduous trees such as birch (e.g., Betula ermanii,
up to 30m). Massive deforestation particularly in coastal zones has led to lack
of supply source of soluble Fe. Urban land expansion in coastal zones and hardening
of coastal areas by hard defense structures (e.g., breakwaters, seawalls, dykes
or other armoured structures) have caused the interruption of Fe supply pathway from terrestrial primary productivity to
the oceans.
Organic matter required to support marine primary
production are supplied within the euphotic (sunlit) zone by a ‘recycling’ of
nutrients (Field et al. 1998; Raven and Falkowski 1999), and are provided from
organic matter sinks in the deep ocean by the transient physical processes,
such eddies, coastal upwelling, and wind or convective mixing (Field et al.
1998; Falkowski et al. 1998; Falkowski 2002). However, a significant fraction
of organic matter from terrestrial primary productivity is exported and sinks
in oceans, sequentially the nutrients are used by primary production in the
ocean euphotic zone (Raven and Falkowski 1999).
Coastal forests play a crucial role in
biogeochemical connectivity between land and sea, by the supply of essential
elements such as organic silicon ‘Si’ and iron ‘Fe’ compounds. Humus and
organic matter such as leaf litter that falls into coastal seas from coastal
forests facilitates the resilience of seagrass meadows, kelp forests, and
diatoms-dominated phytoplankton.
Solutions for eutrophication: closing biogeochemical cycles between land and ocean. There is mounting evidence that excessive nutrient inputs (fertilizer runoff from agriculture, treated sewage discharge and combined sewer outfall, and urban stormwater) lead to harmful algal blooms (e.g., Anderson et al. 2008; Heisler et al. 2008). Furthermore, nutrient pollution is causing the widespread degradation of nearshore ecosystems, including salt marshes (Deegan et al. 2012), mangroves (Lovelock et al. 2009), seagrasses (Orth et al. 2006; Waycott et al. 2009; Jones and Unsworth 2016), and kelp forests (Filbee-Dexter and Wernberg 2018; Feehan et al. 2019).
Seagrass
meadows are considered as biological sentinels, or “coastal canaries” (Orth et
al. 2006), owing to the importance of these ecosystems that support fisheries
production. Nutrient pollution from sewage and livestock waste enhances
excessive growth of epiphytes (microscopic algae) on seagrass leaves,
smothering and decreasing seagrass’s ability to capture light (Jones and Unsworth
2016).
Globally,
canopy-forming kelp forests have been replaced by mats
of turf-forming algae or turfs (a diverse group of
macroalgae). Eutrophication, including sewage and urban pollution, reduces
light penetration in coastal waters and turfs outcompete canopy-forming kelps by
the turfs’ high growth rates and rapid nutrient-uptake rates (Filbee-Dexter and
Wernberg 2018; Feehan et al. 2019).
Wastewater treatment plants
are common worldwide and a required process to improve the quality of
wastewater before it is discharged to water bodies. However wastewater
treatment plants discharge significant quantities of nutrients (Howarth et al.
2002; Carey and Migliaccio 2009). A crucial challenge in nutrient loading is increasing
recycling and safe reuse of human excreta (e.g., van Puijenbroek et al. 2019),
as eutrophication is amplifying the risks of climate change via rising sea
surface temperatures, increased evaporation
from the oceans, and decreased CO2 sequestration.
The key to solving eutrophication is to keep large quantities of undesirable nutrients on the land out of the sea. Comprehensive land-use planning and management that close the land and ocean biogeochemical cycles need to be developed (Tilman et al. 2001; Diaz and Rosenberg 2008).
![]() |
Fig. 3 Nihon-bashi (Tokyo: 35°41′N, 139°46′E) from the series Famous Places in the Bay Capital, Hiroshige, originally published mid-1830’s to early 1840’s (Image courtesy of the British Museum: https://www.hiroshige.org.uk by Chiappa JN). A perspective view from the Nihon-bashi Bridge (the important commercial center in Edo) with a distant Mount Fuji, farsighted the Edo Castle (now the Imperial Palace). On the north bank of the bridge, there lay the largest fish-market in the Edo period, known as Uogashi (魚河岸). Hiroshige depicts natural abundance of marine fishery resources: Retailers with baskets full of fresh fish and all manner of seafood slung over their shoulders head for all parts of the city after making their purchases. Notably, two of Pacific bluefin tuna (Thunnus orientalis, up to 3m or 9.8ft) are carrying with a wooden pole. In Edo, Tuna was common and highly prized for Japanese cuisine sashimi and/or Edo-style sushi. The coherent coastal national strategy leaded to abundant and diverse fish resources, which in turn attracted large pelagic predators such as Tuna. |
6. Comprehensive land-use planning/management in Eastern philosophy: For keeping cool, clear and clean waters
High
primary productivity of vegetation over large geographic areas.
Japan had an abundance of diverse fisheries resources
(Fig. 3). Acknowledged that abundance of fisheries resources is supported by
self-organizing ability of ecosystems, the approaches that had been adopted for
fisheries resources management was unique: comprehensive land-use
planning/management. In Eastern philosophy, land-use
planning/management of high
primary productivity of vegetation over large geographic areas was considered the first principle,
part of the critical infrastructure for socio-economic sustainability via food
security. The philosophy was documented in the early Edo period, by Banzan
Kumazawa (熊沢蕃山, 1619–1691). His theory emphasizes
importance of forestry development and riparian forest
restoration over the whole country (e.g., Sansom 1963)
owing to their synergistic functions: Forests play a key role in moderating
temperatures, keeping soil, groundwater, and running water in rivers/streams cool;
forests stabilize the soil, preventing erosion, in turn contribute to reduction
of sedimentation type pollution keeping clear waters. Notably, mixed
broad-leaved early successional secondary forests dominated by deciduous oaks
(e.g., Quercus serrata, up to 25m or 82 ft; Quercus crispula, up
to 35m or 115 ft) are effective in these functions.
Clean
seawaters: governance approaches in closing
biogeochemical cycles. All living things are made of one
or more cells, and all the cells are mostly composed the same substances that
carry out similar life functions. When the living cells complete their life
cycle, all the essential elements of cells tend to circulate in the biosphere,
known as biogeochemical cycle. In Eastern philosophy, one of the important
concepts of land-use planning/management was to close biogeochemical cycle,
calling rinne輪廻: ‘cycle of life.’
Edo’s
management of human excreta/sewage and waste. The underlying challenges of oceans—eutrophication,
rising sea surface temperatures, harmful algae blooms—require solutions of
‘large quantities of nutrients on the land out of the sea’ via comprehensive
land-use planning and management (Tilman et al. 2001; Diaz and Rosenberg 2008).
Management of human excreta/sewage and waste in Edo
is one of encouraging examples of success. In Edo, political decisions were
made to keep clean seawaters, maintaining high standards of hygiene of sea foods. A traditional form of Japanese cuisine such as sashimi
(sliced fresh fish served raw with garnished herbs) and/or Edo-style sushi
(sliced raw/cooked fish/shellfish on an oval-shaped ball of vinegared rice) was
supported by the clean seawater policy (Fig. 4).
As improper waste management
caused hygiene problems and had negative effects in fisheries in the early Edo
period, disposal of any kind of waste to urban areas and
water bodies (rivers/streams and seas) was severely prohibited in 1655 (Endoh 2004). Due to urban expansion of Edo, the
salt marshes of the eastern parts of the Sumida-gawa River had been reclaimed
from around 1596 to meet rapidly increased needs for residential areas.
Household waste (mostly food scraps, paper, wood) from urban area was collected
and used to fill up the salt marshes with a unique way that closed the
biogeochemical cycles.
In Edo, human excreta from urban areas had been
collected and used in agriculture (Tajima 2007). In Edo, clean sea waters were
maintained by the management of waste and human excreta/sewage.
River
engineering and coastal architecture for land-sea interaction dynamics. Photosynthesis
in marine environment requires the essential elements including silicon ‘Si’ compounds and iron ‘Fe’
compounds from land-sea connectivity. Primary production in marine environment
is enormous: Marine phytoplankton produce nearly half of global net primary production each year (Field et al. 1998). While angiosperm-dominated coastal
ecosystems (salt marshes, mangroves and seagrass meadows) are occupied only 0.2
% of the ocean area, the vegetated coastal habitats have been estimated to be
responsible for 50 % of global CO2 sequestration in marine sediments
(Duarte et al. 2005; Duarte 2017). To sustain these huge primary productions, an enormous amount of essential nutrients must be
supplied from terrestrial vegetation.
Rivers/streams are the main transporters of the
organic matter from the terrestrial environment to the oceans. Large quantities of organic matter enter rivers/streams,
subsequently slow decomposition of leaf litter, wood, and other plant parts
constantly supplies as essential nutrients to productivity of estuaries and
coastal zones, without nutrient pollution. Vast areas of coastal forests
play a vital role as nutrient source for the coastal ecosystems of critical
importance. To close biogeochemical cycles between land and ocean, architecture
of connectivity between terrestrial and marine primary productivity is
essential.
In terms
of organic matter supply, the large amounts of essential nutrients equivalent
to approximately half of global net primary production are required. Therefore,
strategies of high primary productivity of vegetation over the whole country and/or
over entire continents are vital for organic matter dynamics by land-sea
interaction.
Noncontiguous
dyke system
to support productive terrestrial ecosystems and to
preserve natural corridors of land-sea linkage. From a viewpoint of the global hydrological cycle, the overall quantity
of freshwater is only about 2.5% and two-thirds of this fresh water is locked
in glaciers and ice caps. Approximately 0.3% of the Earth’s freshwater is held
in rivers, lakes and reservoirs (Shiklomanov and Rodda 2003). This small
fraction of freshwater plays a vital role to support the terrestrial primary
productivity.
Water management is essential for maintaining high primary productivity
of vegetation over large geographic areas. Japan had unique flood-water management to retain water for longer residence time in land over large geographic
areas (e.g., Okuma 1981). Unique noncontiguous dyke system was developed by
Japanese architects to sustain productive terrestrial ecosystems and to
preserve natural corridors of land-sea linkage (Fig. 6, 7, 8).
Strategical
allocation of vast areas of riparian zones. Stratified foliage of riparian forests shields solar
radiation, which in turn keeps river water cool. The large quantity of leaves,
twigs, and other types of organic matter from riparian forests provides
favorable form of nutrient for freshwater phytoplankton, the basis of stream food webs. Slow decomposition of leaf-litter constantly
supplies essential nutrients without “nutrient pollution.”
Many fish species of commercially importance require
habitats of linkage between river and sea: anadromous
fish migrate from the sea up into fresh water to spawn, such as salmon, Shishamo
(柳葉魚, Spirinchus lanceolatus), striped
bass (Morone saxatilis),
and alewife (Alosa pseudoharengus); catadromous
fish migrate from fresh water down into sea to spawn, such as eels, flathead
grey mullet (Bora, 鰡, Mugil
cephalus), and the Japanese sea bass (Suzuki, 鱸, Lateolabrax japonicus). Rivers are migration corridors for both anadromous
and catadromous fishes. The elaborately shaped landscapes of riparian zones
created favorable conditions for freshwater
phytoplankton proliferation, and served as nursery and foraging grounds for
these migratory fishes.
In terms of organic matter supply, high Si accumulation plants of the families of Poaceae (grass family), Equisetaceae (horsetail family) and Cyperaceae (family of graminoid) flourish in riparian zones may play a vital role in silica supply for diatoms (important in marine wood-webs). High primary productivity of forests over large geographic areas yields enormous amount of ‘cytochromes,’ which in turn may contribute to availability of Fe for photosynthesis in marine environment.
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Fig. 5 River divert project in Edo started from around 1594 (a) Location of project sites. (b) Coastal area of Tokyo in 1959 (the Geographical Survey Institute, Japan). A: Imperial Palace (Edo Castle); B: Sumida-gawa River 隅田川; C: Nihon-bashi (important commercial center in Edo); D: Akabori-gawa River, 赤堀川, man-made channel about 8.6km or 5.3mi long to flow out Tone-gawa River to the Pacific Ocean, started from around 1594 completed in 1654; E: levee to check flow for separation of Tone-gawa River and Ara-kawa River in 1629; F: Edo-gawa River, 江戸川, man-made channel to control flood-flow started from 1635 completed in 1654; G: ancient estuary of Sumida-gawa River; H: man-made channel of Ara-kawa River, 荒川放水路, excavated in 1911–1930 from the site I; I: Senjyu Great Bridge, near the branching off point of the man-made channel of Ara-kawa River completed in 1930 from Sumida-gawa River; J: reclaimed marsh land from around 1596; K: hard ground of the Kono-dai plateau; L: Horie and Nekozane, landscaping levee to protect hinterland below sea level; M: hunting reserve for shogun family (currently belonging to the Imperial Household Ministry) |
7.
A
case of successful land-use planning/management: Edo
7.1 The
largest metropolis in the 18th century: Edo
Hiroshige Utagawa (歌川広重, 1797–1858) illustrated many landscape prints depicting land-use
planning/management of Eastern philosophy, owing to his background of samurai: ruling class obliged their duties and moral.
Japan had coherent coastal
national strategy until the mid-19th century. Although urban development of
Edo radically changed natural geographical features (http://harukanoor4.blogspot.com/2019/),
decisions were made to enhance ecological resilience for
fisheries.
Edo (lit., bay-entrance or estuary) is the former
name of the Japanese capital Tokyo (35°41′N, 139°42′E)
developed at estuaries of Tone-gawa River system, facing on Edo (Tokyo)
Bay. In 1590, Ieyasu Tokugawa (徳川家康1542–1616) settled in Edo, and established his Shogunate (military governing
dynasty) in 1603. Edo began to increase in extent and population, and had over
one million inhabitants as early as the middle of the eighteenth century,
making it the largest metropolis in the worlds (Sansom 1963; Uspensky 2003).
In Fig. 3, Hiroshige depicts a
perspective view from the Nihon-bashi Bridge (the important commercial
center in Edo) with a distant Mount Fuji, farsighted Edo Castle (the current Imperial
Palace). On the north bank of the bridge, there lay
the largest fish-market in the Edo period, known as Uogashi (魚河岸).
It must be early in morning: fishmongers
with baskets full of fresh-caught fish and other seafood slung over their
shoulders head for all parts of the city, after making their purchases.
Notably, two of Pacific bluefin tuna (Thunnus orientalis, up to 3m or
9.8ft) are carrying with a wooden pole. In Edo, Tuna was common and highly
prized for Japanese cuisine sashimi and/or Edo-style sushi. The coherent coastal national strategy
leaded to abundant and diverse fish resources, which in turn attracted large
pelagic predators such as Tuna. Accordingly, off-shores of Edo were good
fishing spots for Tuna.
7.2 Ambitious divert project of Tone-gawa
River in Edo
To reduce flood-risks in Edo, an ambitious project
to divert the flow of the Tone-gawa River was
accomplished (Okuma 1981). In ancient times, several distributaries of Tone-gawa
River, forming meandering streams with no firm channels, flowed
into Edo Bay. The Sumida-gawa River was one of the distributaries
flowed into Edo Bay. As soon as Ieyasu settled in Edo in 1590, he started to
the extremely complicate project of river diversion.
In 1594, one of the main flows of the Tone-gawa
River was checked by a levee structure at a site of the upper stream (熊谷, Kumagaya, around 70km or 44mi from Edo Bay; 36°11′N, 139°31′E). Thereafter two stream channels were
excavated: Shinkawadoori (新川通8km or 5mi long; width: 18m or 59ft in 1621)
was followed by Akahori-gawa (赤堀川about 8.6km or 5.3mi long, width: 18m in 1654). (These man-made
channels were widened to 72m or 236ft and deepened until 1809.) By the excavation work of the channel Akahori-gawa
(Fig. 5, D), the main flow of Tone-gawa River was connected with Hitachi-gawa
River that pours into the Pacific Ocean. Accordingly, the flows of the two
rivers were merged into one huge flow, which discharges into the Pacific Ocean
(Fig. 5).
Simultaneously, a river
system of the Sumida-gawa River was separated from the Tone-gawa
River system to reduce flood risks in Edo area. In ancient times, the Sumida-gawa
River was one of several distributaries of Tone-gawa River flowed into
Edo Bay. Flow from the Tone-gawa River system was checked by a levee
structure at a point of the upper stream (Kumagaya, 熊谷, about 64km or 40mi from Edo Bay; 36°13′N, 139°40′E;
Fig. 5, E) in 1629. Accordingly, a distributary system (Ara-kawa River, 荒川) was separated from Tone-gawa River. Which in turn decreased
volume of water flow to Edo area. As so often with Edo’s rivers, it had a local name
in Edo—Sumida-gawa River (Fig. 5, B). (To reduce flood risks in Tokyo,
man-made channel of Ara-kawa River, 荒川放水路, was excavated in 1911–1930. Hence, the Sumida-gawa River branches off
from the Ara-kawa River shown in Fig. 5, I.)
In addition, a man-made
channel, from the main stream of the Tone-gawa River to Edo Bay, was excavated to control flood-flow (江戸川, Edo-gawa River about 18km or 11mi long; Fig. 5, F) in 1635. For
the excavation work of the channel to flow out flood waters toward the
outskirts of Edo, natural courses of a distributary system were partly used,
besides sites of hard ground were selected to stabilize the stream flow (Fig. 7-1).
Eventually, a series of the river diversion works
and the excavation works of the channels contributed to an element of
importance in Edo’s waterborne transport system (Okuma 1981). Owing to its military importance, a
hunting preserve for the shogun family was placed at the estuary (Fig.5, M). As
forbidden land, coastal forests and wetlands were maintained. Notably, a
variety of habitats for fisheries were elaborately shaped in the landscape
architecture of the river divert project, as Hiroshige depicts: e.g., Sumida-gawa
River (Fig. 6), man-made channel of Edo-gawa
River (Fig. 7), and coastal engineering of estuarine of Edo-gawa
River (Fig. 8).
Fig. 6-1 Senju Great Bridge (Tokyo: 35°44′ N, 139°48′ E) from the series One Hundred Views of Edo, Hiroshige, originally published 1856–59. Japanese architects developed unique ‘dam’ system to retain flood-water on the either side of the river in desolate areas. An extensive area of flood-water retarding zone checked by embankment enables allocated vast areas of riparian forests, and preserves natural drainage corridors of land-sea linkage for abundant supply of organic matter. This bridge in the outskirts of Edo over the Sumida-gawa River (Fig. 5, I) was built in 1594 using wood of the evergreen yew plum pine (Podocarpus macrophyllus, up to 20m, endemic to the ancient supercontinent of Gondwana). The wood did not rot over 300 years, owing to resistance to rot and termites. In ancient times, the Sumida-gawa River was one of several distributaries of Tone-gawa River poured into Edo Bay. To reduce flood risks in Edo, the Sumida-gawa River was separated from the Tone-gawa River system in 1629, by construction of a levee to check flow of the Tone-gawa River system at a site (Fig. 5, E, about 64km or 40mi of upper-stream). Eventually, the Ara-kawa River originates from the Chichibu-santi mountain chain ran in Edo. As so often with Edo’s rivers, it had a local name in Edo—Sumida-gawa River. Hiroshige depicts corridor architecture of land-sea linkage. Cool river water originates from deep forests of distant Mount Buko meanders along contiguous deep riparian forests. The cool river water in turn cools coastal seawater together with supply of important terrigenous organic matter, including silica within the plant cell wall and soluble Fe in cell structure, which are required to support marine primary productivity. |
7.3
Land governance and unique
design of river engineering to maintain cool, clean and clear waters
7.3.1
Total land-use planning/management.
In Eastern philosophy, sustaining forests from mountainous areas of river
headwaters toward coastal areas and watershed management of running clear
waters were regarded as the first principle in the critical infrastructure for
sustainability of society. In Fig. 6-1, Hiroshige depicts a perspective view form the Senjyu-Ohashi
Bridge built in 1594, the first and largest bridge over the Sumida-gawa River with a distant Mount Buko (elevation: originally 1,336m or
4,383ft, Fig. 5a), one of the peaks of the Chichibu-santi mountain chain.
In 1629, in one phase of the series of the large-scale river diversion works
(Fig. 5), Ara-kawa River was separated from
the Tone-gawa River system by a levee (Fig. 5, E, about 64km or 40mi
from Edo Bay). The Ara-kawa River originating from the
Chichibu-santi
mountain chain ran in Edo (local name of the Ara-kawa River
in Edo—Sumida-gawa River). Since
ancient times, the Chichibu-santi mountain chain, the
headwaters of the Ara-kawa River, had been the subject of sacred
mountain religious worship.
Shugendo (修験道, meaning “the path of training and testing”),
founded by En no Ozunu (役小角 or En no Gyoja 役行者, 634–701), was later combined with Buddhism mainly
the Shingon Sect established by Kūkai (空海, 774–835). The deep old-growth forests were maintained as forbidden land
over a millennium, allowing only shugenja (修験者, Shugendo monks) to enter these areas
for their religious experience/training (http://harukanoor4.blogspot.com/2016/).
As monks of Shugendo devoted to helping people via medication using
diverse herbs gathered from the sacred mountains along with performance of
Buddhist rituals, people adored them.
The mountains of Chichibu-santi
are incorporated in their myths and legends as sacred sites: The name of Mount Buko has a legendary explanation.
Fascinated by the imposing mountain, the legendary Prince Yamato-takeru (http://harukanoor4.blogspot.com/2019/)
ascended the mountain, and he dedicated his armor helmet (甲) to the spirit of mountains. This was taken up as Buko
(武甲, brave armor helmet) and became a name of the
mountain. It was noted for the cool artesian springs. In ancient times, En
no Ozunu often visited the deep old-growth forests for his religious
experience/training.
On the other hand, the foothills were venues for
numerous pleasurable activities for people. Pilgrimage
in Japan has its roots in ancient times, by the Edo period pilgrimages had
become generally practiced. A route of Chichibu Pilgrimage along the
foot of Mount Buko, a multi-site pilgrimage of 34 temples, was noted for
the beauty of the surrounding countryside and traditional inns with hot springs
and bathing facilities. The pilgrim of roughly 100km
(62mi) long way near Edo became exceptionally popular.
In terms of land-sea interactions, deep old-growth forests forming the headwater sources play a profound role. For the abundance and high primary productivity of marine phytoplankton, large quantities of the essential elements such as iron ‘Fe’ compounds are supplied from the high primary productivity of forests to the productive ocean margins. The stratified canopy foliage of deep forests shields solar radiation, which in turn keeps soil moisture and groundwater cool. As a significant amount of the water flowing in rivers comes from groundwater, cool groundwater discharge into river streams keeps stream water cool. The inflow of cool river water makes an important contribution to marine primary productivity, providing favorable temperature conditions for productive diatoms-dominated phytoplankton blooms.
![]() |
Fig. 6-2 Sekiya Village from the series Thirty-six Views of Eastern Capital, Hiroshige Ⅱ (1826–1862), originally published 1861–62 (Image courtesy of the National Diet Library, Japan). Salt-marshes along the ancient estuarine of the Sumida-gawa River had been reclaimed from around 1590. To reduce flood hazards in urban area of Edo, an extensive area of flood-water retaining zone was allocated here (Fig. 5, G). Owing to abundant organic matter supply by floods and retaining soil moisture, the man-made flood recurring zone was very fertile. Vegetables of all sorts were grown. Sekiya village was also noted for its abundant fisheries resources, as intricate channels from the Sumida-gawa River to diffuse flood-waters into low-lying plains and numerous man-made sandbanks covered with dense riparian forests to dissipate flood-water wave-energy created diverse habitats for resilient inland fisheries. The benefits of the flood recurring zone, local societies and economics supported by high productivity, balanced with the threats posed by floods. |
![]() |
Fig. 6-3 Sekiya Village on Sumida-gawa River from the series Thirty-six Views of Mount Fuji, Hokusai Katsushika (1760–1849), originally published around 1831 (Image courtesy of the Adachi Institute of Woodcut Prints https://www.adachi-hanga.com/). In outskirts of Edo, an extensive area of flood-water retarding zone was allocated on either side of the Sumida-gawa River. Senju Great Bridge (Fig. 6-1) was positioned in the flood-water retarding zone. Flood-waters were allowed to flow into the low-lying plains of ancient estuarine of the Sumida-gawa River. To check the flood-waters, this meandering embankment (distance from the Senju Great Bridge, around 1,650m or 1mi) was built in 1616. Hokusai depicts the embankment, featuring the unique shape and the vastness of the flood-water retarding zone. |
7.3.2
Unique design of river engineering
Noncontiguous
dike system
in Edo. Noncontiguous dike system to retain flood-waters in desolate areas was ordinarily
adopted in river engineering in the Edo era. In this system, an extensive area of flood-water retaining zone was
allocated, which in turn enabled placement of vast areas of riparian
forests and wetlands.
Flood-water
retaining system
served as a sort of ‘dam’ not to block river. To decrease peak discharge, volume, and frequency of
floods in urban area of Edo, an extensive area of flood-water retarding zone was strategically allocated on either side of the upper-stream of the Sumida-gawa
River. The Senjyu-Ohashi Bridge (Fig. 5, I; Fig. 6-1) was
situated in the flood-water retarding zone in the
outskirts of Edo. Landscape architecture of the
man-made flood recurring zone was depicted by Hiroshige
Ⅱ (1826–1862) (Fig. 6-2).
The large tracts of salt-marshes extended along Edo Bay
at the ancient estuarine of the Sumida-gawa
River (Fig. 5, G) had been reclaimed from around
1590 (Endoh 2004). To retain flood-water, long embankments in slanted angle to
the river flow were raised from a point of the ancient estuarine, and low-lying
flood plains were semi-enclosed by the embankment.
The V-shaped embankment on the either side of the Sumida-gawa
River served as a sort of ‘dam.’
When Ieyasu settled in Edo in 1590, the embankment system in left
side of the river from Kumagaya (熊谷, about 60 km or 37 mi upper-stream) to the point (Fig.
5, G) was already partly existed. The meandering
embankment (Fig. 6-3, length: 3.8km or 2.4mi, distance
from the Senju-Ohashi Bridge: around 1,650m
or 1mi) was built in 1616. Hokusai depicts the meandering embankment, featuring
the uniqueness of the shape and the vastness of the flood-water retaining
zone.
Some quarters of Asakusa (right side of the
river) had been seriously affected by flooding of the Ara-kawa River. In
1620, an embankment (length: 860m or 0.53mi; height: 3m or 9.8ft; width of
levee crown: 7.2m or 24ft) along a moat connecting the Musasino Plateau
was constructed. Flood-waters overflowed in the outskirts of upper-stream Asakusa,
and prevented recurrence of flooding in important areas of Asakusa.
In Fig. 6-1, Hiroshige depicts
a view of the Sumida-gawa River in the flood-water
retarding zone. A series of man-made sandbanks that
directed water-flows into low-lying plains are constructed as parallel each
other with a slanted angle.
Architecture of
flood-water retarding zone. In Fig. 6-2, Hiroshige Ⅱ depicts the man-made flood recurring zone, just
across the Senju-Ohashi Bridge from Edo. The existence of the Sumida-gawa
River is indicated by the sail of ships, beyond dense riparian forests and
constructed wetlands. To diffuse flood-waters toward into low-lying plains, intricate channels from the Sumida-gawa
River are excavated. Numerous Man-made sandbanks are raised to dissipate
flood-water wave energy.
Strategically allocated vast areas of riparian zones
are able to perform ecosystem functions of retaining and filtering
flood-waters, while keeping organic matter dynamics by land-sea interactions. To construct irregular-shaped wetlands covered with common reed (Phragmites
australis), closely spaced wooden piles made from pine wood were driven
into the riverbed. Pine wood does not rot in wet and oxygen-poor conditions and
become as hard as stone when left in immersed in water. Along
the wetlands, numerous ‘loosing spaced wooden piles’ driven into riverbed
served as a sort of breakwater, preventing the bank from being washed away by
the strong current (http://harukanoor4.blogspot.com/2019/).
The man-made
flood recurring zone was very fertile, as flood-waters carried abundant organic
matter and distributed it across a wide area. Sekiya village was noted for its production
of all sorts of vegetables and abundant inland fisheries
resources. Created open space of vast emptiness provided venue for
pleasurable activities for people (Fig. 6-2, 6-3).
Flood-water
retaining
system in man-made channel of the Edo-gawa River.
As part
of the ambitious river divert project, Edo-gawa River (Fig. 5, F) was
excavated to redirect Tone-gawa River flood waters to the outskirts of
the Eastern Capital, in 1635 (Okuma 1981). In the excavation work of flood-flow
control, a site of hard ground was selected. Hard ground of Kono-dai
Hill in the foreground in Fig. 7-1 served as a sort of ‘rigid structure
of dyke.’ On the
other side, an extensive area of flood-water retaining zone was allocated in
the west-side of the Edo-gawa River. Numerous man-made sandbanks that directed
water-flow into low-lying plains are raised together with dense riparian
forests and constructed wetlands.
Need for land governance. Land-use planning is connected important policy issues: flood management, aquatic resource management for food security, and CO2 sequestration in a vast area of ocean. Edo’s flood-water retaining zone projects suggest that a multidimensional approach is required with a wide range of policies.
![]() |
Fig. 7-1 The Edo-gawa River at Kono-dai Hill (Chiba: 35°45′ N, 139°54′ E) from the series Thirty-Six Views of Mount Fuji, Hiroshige, originally published 1852 (Image courtesy of the British Museum: https://www.hiroshige.org.uk by Chiappa JN). The Edo-gawa River (Fig. 3, F) was excavated to flow out flood-waters of the Tone-gawa River to the peripheries of Edo in 1635. To create a firm channel, hard ground of plateau was selected. Earthen groynes (groins), sandbars that extended into river from river-shore, were constructed in the man-made meandering channel. The landscaping groynes covered with riparian forests were fringed with constructed wetlands created by closely spaced wooden piles driven into riverbed. ‘Loosely spaced wooden piles’ driven into riverbed served as a sort of breakwater, preventing the shorelines being washed away. These river engineering structures create a variety of habitats: riffles, calmer flows, and deep pools. Man-made riffles serve to aerate the running river water by babbling currents, increasing the amount of dissolved oxygen. Diatoms-dominated freshwater phytoplankton, the basis of stream food webs, thrive better in cool, clear, clean, and oxygen-rich waters. In Eastern philosophy, unique design of river engineering had been developed taking into account of aquatic resources management.
7.3.3 Maintaining freshwater quality: The landscaping river groynes serve to aerate the cool river water.
Biological processes in the integrity of terrestrial
and aquatic ecosystems, constituting a complex and dynamic system, play a
pivotal role in qualitative restoration of freshwater. In Eastern philosophy, unique
design of river engineering had been developed to maintain
freshwater quality.
In recent decades, toxic cyanobacterial blooms
represent a serious threat for water quality of surface waters worldwide (e.g, Paerl
and Huisman 2008). In stagnant waters like lakes, ponds, or reservoirs, toxic
cyanobacteria thrive better under the condition of excessive nutrients
(fertilizer runoff from agriculture, sewage and industrial discharges, and
urban stormwater) in warmer water temperatures.
In Fig. 6-1, 7-1, 7-2, Hiroshige depicts a unique
design of river engineering: irregular-shaped river
groynes covered with riparian forests. These sandbars, that extend into river, create a variety of habitats: riffles (瀬), calmer flows, and deep pools (淵). Man-made riffles serve to aerate the cool running river water by babbling
currents, increasing the amount of dissolved oxygen. Diatoms-dominated
freshwater phytoplankton, the basis of stream food webs, thrive better in cool,
clear, clean, and oxygen-rich waters. Even in construction of man-made channel of Edo-gawa
River, the landscaping earthen groynes covered with
riparian forests fringed with constructed wetlands were created.
In land governance of Eastern philosophy, ‘steady
streaming water flows’ and ‘babbling currents’ were highly prized for the
function of maintaining freshwater quality. From the Edo period onward, ‘civil
engineering’ is referred to doboku土木working with
earth and trees/woods. Japanese engineers pursued aesthetic works in
river engineering using earth and trees/woods.
![]() |
Fig. 7-2 Scattered Pines,
Edo-gawa River from the series One Hundred Views of Edo, Hiroshige,
originally published 1856–59 (Image courtesy of the Adachi Institute of Woodcut Prints https://www.adachi-hanga.com/). Hiroshige
depicts a near estuaries landscape of man-made channel
of the Edo-gawa River. The net being cast in the foreground and the
fishing boat that part of it seen through the net imply abundance of fisheries
resources. The fishermen are working along the constructed reedbeds. The river engineering of Eastern philosophy, the deep
riparian forests in the backdrop of this print and earthen groynes with pine
groves fringed with reedbeds, created a man-made channel of abundant fisheries
resources. |
7.4
Coastal landscape architecture for keeping cool,
clean and clear seawaters
7.4.1
Coastal protection integrated with diverse habitats for resilient fisheries.
At the river mouth of the Edo-gawa River,
excavated in 1635 to discharge flood waters of Tone-gawa River to the
remote coast from the heart of the city of Edo (Fig. 5, F), coastal landscapes
were shaped by unique design of coastal engineering in Eastern philosophy.
As the Japanese archipelago is prone to tropical
cyclone and tsunami, ancient Japanese architects were aware that local
geographical features such as island and/or coastal hill/mountain contribute to
coastal protection by reducing wave energy. Through
the learning-based approach over millenniums via dialogue with dynamic
earth-surface system, designs and techniques in shaping landscapes contribute
to coastal protection by reducing wave energy were developed. Japan had unique
design and techniques in construction of coastal protection integrated with a
variety of habitats for resilient fisheries.
Hiroshige depicts landscapes of estuarine zone of the
man-made channel of Edo-gawa River that intricately shaped by humans, Gyotoku
(行徳, Chiba, 35°41′ N, 139°54′ E), featuring unique
design of coastal and estuarine engineering (Fig. 8).
When Ieyasu settled in Edo in 1590, the mouth of the
Sumida-gawa River was situated in north-east site of the Edo Castle (Fig. 3, I). At that time, Gyotoku was an
island. The estuarine zone near the mouth of the Edo-gawa River covered
by large tracts of salt marshes and mud flats was reclaimed from around 1596 (Fig.
5, J) (Endoh 2004).
In Fig. 8-1, Hiroshige
depicts a distant view of the unique feature of irregular-shaped embankment
system from the hinter land. Gyotoku was
noted for its salt production. Beyond the irregularly bending dyke that local villagers walking along it with their carrying poles, the salt beach
is spreading. On the solar evaporation pans the workers occupy with obtaining
salt. On the right the embankment projects into the broad forested coastal
hills at the river mouth. The unique design of the embankment
system in the estuary of the man-made channel of Edo-gawa River: irregularly bending
dyke and forested coastal hills that project into sea were effective in dissipating wave energy of
tropical cyclone, storm surge and tsunami.
![]() |
Fig. 8-1 Salt Beach at Gyōtoku (Chiba, 35°41′ N, 139°54′ E) from the series Famous Views in the Vicinity of Edo, Hiroshige, originally published 1839 (Image courtesy of the Museum of Fine Art, Boston). In 1635, the Edo-gawa River (Fig. 5, F) was excavated to flow out flood-waters of the Tone-gawa River to the outskirts of the Eastern Capital. Large tracts of salt marshes in the man-made channel’s estuarine areas were reclaimed from around 1596. Hiroshige depicts a distant view of the unique design of the embankment system in the estuary of the man-made channel: irregularly bending dyke and broad forested coastal hills that project into sea. |
In Fig. 8-2, Hiroshige
depicts the mouth of the Edo-gawa River from offshore. To reduce wave energy, Japanese engineers often placed
man-made islands in entrance of bay and/or river mouth. Behind the passenger
boat in the foreground, a man-made island fringed with irregular-shaped man-made
sandbanks is placed. The
man-made island served as a sort of caisson
breakwater, absorbing wave energy and providing safe
harborage. To create the island, closely spaced pine
piles were driven into sea-floor. Along the man-made sandbanks, numerous ‘loosing
spaced wooden piles’ are driven into sea-floor served as a sort of breakwater
to reduce the intensity of wave action and thereby reduce erosion.
At the upper right of this print, the town of Gyotoku
lay behind large expanses of ‘solar evaporation salt pans’ with pine trees
evenly spaced along the bank. The tall and dense coastal forests at the upper left of this print were belonged to villages of Horie and Nekozane (Fig. 3, M), depicted
as the broad forested coastal hills. The coastal shoreline was shaped by the
techniques of closely spaced pine piles driven into sea-floor and ‘loosing
spaced wooden piles’ breakwaters.
![]() |
Fig. 8-2 Returning Sails at Gyotoku from the series Eight Views of the Environs of Edo, Hiroshige, originally published mid-1830’ (Image courtesy of the National Diet Library, Japan). Hiroshige depicts a view of the irregular-shaped embankment system, broad forested coastal hills that project into sea (Fig. 8-1), from offshore of the mouth of the Edo-gawa River. To dissipate wave energy, Japanese engineers often placed man-made islands at the entrance of bay and/or river mouth, serving as a sort of caisson breakwater. The estuary architecture of coastal protection, the broad forested coastal hills and man-made island surrounded with irregular-shaped sandbanks, performs function of organic matter dynamics by land-sea interactions. |
7.4.2
Land-sea connectivity via non-fragmented
ecosystems
Construction of
a variety of habitats: Intricate estuarine
channels, man-made sandbanks, mudflats, man-made islands, and salt
marshes. In Fig. 8-3,
Hiroshige depicts a closer view of the unique feature of embankment
system in Horie and Nekozane.
At the river mouth, the man-made channel of Edo-gawa
River divides into two branches so as to form two forks. Two villages, Nekozane
on right and Horie on the left of the Sakai-gawa canal (a branch
of the Edo-gawa River), are depicted from the direction of Edo Bay. The
existence of the Edo-gawa River is indicated by the masts of two boats
seen in the depths of the print below with dense riparian forests on the other
side of the river, to the right of Mount Fuji.
The name Nekozane is derived from a folk-lore:
in the era of the Kamakura shogunate (1185–1333), local people, who suffered recurrent
coastal floods, raised the ground level and constructed hills. Pine trees (Pinus thunbergii) were planted on the hills. The dike system was
very effective to absorb storm energy, hence wave overtopping of
tsunami/cyclone did not pass over (kosanu, 越さぬ) the tree bases (ne, 根) of the pine trees: ‘ne kosanu’ changed to ‘Nekozane.’
A prized clam (Mactra chinensis), supplied to
city market from these two villages, was popular as topping of Edo-style sushi
known as aoyagi, 青柳. The clams were gathered on the many man-made
sandbanks. In Fig. 8-3, the presence of local villagers on the levee road
indicates height of the hill embankment. A gentle slope run up from the dyke to
the precincts of the shrine, shielded with tall and dense sacred groves.
Placement of
non-fragmented ecosystems for land-sea connectivity. Estuarine
and coastal ecosystems play a significant role in closing biogeochemical cycle of land-sea
connectivity. Continuous vegetation: dense estuarine forests (Fig. 8-3), man-made
islands/coastal hills covered with thick coastal forests (Fig.
8-2) and lush tidal marshes, facilitates habitat connectivity between land and sea,
leading to the resilience of seagrass meadows and
kelp-forests. As biochemical materials such as silicon ‘Si’ compounds and
iron ‘Fe’ compounds are supplied from estuarine and coastal vegetation, high productivity of marine photosynthesis of seagrass
meadows and kelp-forests maintains and recovery from disturbance is easy.
Japanese engineers constructed extensive salt
marshes that fringe man-made island (Fig. 8-2) and coastal hills (Fig. 8-3). Salt
marshes act as natural filter that trap sediments and purify seawater (e.g., Barbier
et al. 2011), reducing sedimentation type pollution and enhancing clarity of seawaters.
Estuarine and coastal ecosystems control seawater
temperatures via foliage shield effects, solar radiation balance, and cool
groundwater discharge to coastal seas (Fig.1).
Countless sandbanks along with numerous ‘loosing
spaced wooden piles’ driven into sea-floor served as a sort of breakwater
create a variety of habitats: riffles, calmer flows, and deep pools. These
man-made structures serve to aerate the cool seawaters by babbling waves,
increasing the amount of dissolved oxygen.
Offshore of Gyotoku was noted for its high quality fisheries resources, and was esteemed as one of Osaiura (御菜浦, His Excellency’s fishing zones). This fact suggests that the landscape elaborately shaped by humans created resilient sea: diatoms-dominated phytoplankton, the basis of marine food webs, flourished in cool, clear, clean, and oxygen-rich seawaters, with huge amounts of organic matter (e.g., leaf litter, wood, other plant parts, and humus) supply from coastal vegetation; flourishing seagrass meadows and kelp-forests provided fish and invertebrate nursery ground and foraging.
![]() |
Fig. 8-3 Villages of Horie and Nekozane from the series One Hundred Views of Edo, Hiroshige, originally published 1856–59 (Image courtesy of the British Museum: https://www.hiroshige.org.uk by Chiappa JN). In a closer view of the broad forested coastal hills in Horie and Nekozane, Hiroshige depicts the estuary landscape architecture that enables organic matter dynamics by land-sea interactions. Aware that lush landscapes of estuaries and coastal zones play an important role in marine photosynthesis and fisheries, a variety of habitats were elaborately shaped: man-made sandbanks, mudflats, man-made islets, salt marshes, and thick coastal forests. The coastal fishery villages were renowned for its supply of a particular edible clam (Mactra chinensis), popular as topping of Edo-style sushi, gathered on the many man-made sandbanks. Because of the excellent point for gathering shellfish and fishing, the coastal sea of the man-made channel of Edo-gawa River was designated as one of Osaiura, 御菜浦, His Excellency’s fishing zones. The catches were delivered to shogun’s court. |
8. Land
governance and climate
change
Photosynthesis in marine environment heavily
distributes in the coastal areas, that covers less than 10% of the world ocean.
The dynamic biological process of marine photosynthesis influences climate, via
CO2 sequestration in the deep sea (phytoplankton:
Field et al. 1998, Falkowski et al.
1998, Falkowski 2002; coastal vegetation: Duarte et al. 2005, Duarte 2017) and via solar
radiation valance (Fig. 1). Decline of photosynthesis in the coastal area
allows increase in sea temperatures and causes amplified evaporation from the
oceans.
In Edo, the approaches that had been adopted to
manage fisheries resources for food security were unique and effective. The diatoms-dominated
marine phytoplankton, the basis of abundant fisheries resources, requires supply
of essential elements such as iron ‘Fe’ and silica ‘Si’ compounds from
terrestrial vegetation, in addition to cool, clear, clean seawaters. To meet
the basic requirements, policy of human excreta management and watershed
management sustaining forests along with running waters were implemented. The unique
design and techniques of river/coastal engineering, closing the biogeochemical
cycles and maintaining organic matter dynamics by land-sea interactions had
been developed.
The Edo’s estuarine and coastal transformation by
humans created diverse and productive habitats. The abundance and high primary
productivity of marine environment led by the land governance of Edo, in turn,
contributed to reducing negative impacts on climate. The unique learning-based
approach in Eastern philosophy provides guidance for productive future, as
fisheries resource management integrated with climate change
mitigation/adaptation is a major global challenge.
References
Alongi DM (2014) Carbon cycling and storage in mangrove forests. Annu. Rev. Mar.
Sci. 6:195–219. doi: 10.1146/annurev-marine-010213-135020
Anderson DM, Burkholder M, Cochlan WP, Glibert PM,
Gobler CJ, et al. (2008) Harmful algal blooms and eutrophication: Examining
linkages from selected coastal regions of the United States. Harmful Algae.
8:39–53. doi:10.1016/j.hal.2008.08.017
Anderson DM, Alpermann TJ, Cembella AD, Collos
Y, Masseret E, Montresor M (2012) The globally distributed genus Alexandrium:
multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10–35. doi:10.1016/j.hal.2011.10.012
Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192.
doi:10.1038/nature08057
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR
(2011) The value of estuarine and coastal ecosystem services. Ecol. Monogr.
81:169–193. doi: 10.1890/10-1510.1
Bates SS, Garrison DL, Horner RA (1998) Bloom dynamics and
physiology of domoic-acid-producing Pseudo-nitzschia species. In:
Anderson DM, Cembella AD, Hallegraef GM (Eds.), Physiological Ecology of
Harmful Algal Blooms. Springer-Verlag, Heidelberg, pp. 267–292.
Batistić M, Garić R, Jasprica N,
Ljubimir S, Mikuš J (2019). Bloom of the heterotrophic dinoflagellate Noctiluca
scintillans (Macartney) Kofoid & Swezy, 1921 and tunicates Salpa
fusiformis Cuvier, 1804 and Salpa maxima Forskål, 1775 in the open
southern Adriatic in 2009. J. Mar. Biol. Assoc. U.K. 99:1049–1058. doi: 10.1017/
S0025315418001029
Blackburn GA (2007) Hyperspectral remote sensing of plant
pigments. J. Exp. Bot. 58:855–867. doi:10.1093/jxb/erl123
Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline
over the past century. Nature 466:591–596. doi: 10.1038/nature09268
Boyce DG, Dowd M, Lewis MR, Worm B (2014) Estimating global chlorophyll
changes over the past century. Prog. Oceanogr. 122:163–173. doi: 10.1016/j.pocean.2014.01.004
Bricelj VM, Lonsdale DJ (1997) Aureococcus
anophagefferens: causes and ecological consequences of brown tides in U.S.
mid-Atlantic coastal waters. Limnol. Oceanogr. 42:1023–1038. doi: 10.4319/lo.1997.42.5_part_2.1023
Bricelj VM, MacQuarrie SP (2007) Effects of brown tide (Aureococcus anophagefferens) on
hard clam Mercenaria mercenaria larvae and implications for benthic
recruitment. Mar. Ecol. Prog. Ser. 331:147–159. doi:10.3354/meps331147
Bryan-Brown DN, Connolly RM, Richards DR, Adame F, Friess
DA, Brown CJ (2020) Global trends in
mangrove forest fragmentation. Sci. Rep. 10:7117. doi: 10.1038/s41598-020-63880-1
Butler MH.IV, Hunt JH, Herrnkind WF, Childress MH,
Michael J, et al. (1995) Cascading disturbances in Florida Bay, USA:
cyanobacterial blooms, sponge mortality, and implications for juvenile spiny
lobsters Panulirus argus. Mar. Ecol. Prog. Ser. 129:119–125. doi: 10.3354/meps129119
Carey RO, Migliaccio KW (2009) Contribution
of wastewater treatment plant effluents to nutrient dynamics in aquatic systems:
a review. Environ. Manage. 44:205–217. doi: 10.1007/s00267-009-9309-5
Carmichael WW, Boyer GL (2016) Health impacts
from cyanobacteria harmful algae blooms: Implications for the North American
Great Lakes. Harmful Algae 54:194–212. doi: 10.1016/j.hal.2016.02.002
Carugati L, Gatto B, Rastelli E, Martire ML, Coral S, et al. (2018) Impact of mangrove forests degradation on biodiversity and
ecosystem functioning. Sci. Rep. 8:13298. doi: 10.1038/s41598-018-31683-0
Chen B, Kang W, Guo H, Lin H (2021) Karenia mikimotoi blooms in
coastal waters of China from 1998 to 2017. Estuar. Coast. Shelf Sci. 249:107034.
doi: 10.1016/j.ecss.2020.107034
Conley DJ (2002) Terrestrial ecosystems and the global
biogeochemical silica cycle. Global Biogeoch. Cycl. 16:1121. doi: 10.1029/2002GB001894
Currie HA, Perry CC (2007) Silica in plants: biological, biochemical and chemical
studies. Ann. Bot. 100:1383–1389. doi: 10.1093/aob/mcm247
Davidson K, Miller P, Wilding TA, Shutler J, Bresnan E, et al. (2009) A
large and prolonged bloom of Karenia mikimotoi in Scottish waters in
2006. Harmful Algae 8:349–361. doi: 10.1016/j.hal.2008.07.007
Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, et al. (2012)
Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–392. doi: 10.1038/nature11533
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine
ecosystems. Science 321:926–929. doi: 10.1126/science.1156401
do Rosário Gomes H, Goes JI, Matondkar SGP, Buskey EJ, Basu S, et al. (2014)
Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due
to spread of hypoxia. Nat. Commun. 5:4862. doi:10.1038/ncomms5862
Duarte CM, Chiscano CL (1999) Seagrass biomass and production: A
reassessment. Aquat. Bot. 65:159–174. doi: 10.1016/S0304-3770(99)00038-8
Duarte CM, Middelburg JJ, Caraco N (2005) Major role of marine
vegetation on the oceanic carbon cycle. Biogeosciences 2:1–8. doi: 10.5194/bg-2-1-2005
Duarte CM (2017) Reviews and syntheses: Hidden forests, the role
of vegetated coastal habitats in the ocean carbon budget, Biogeosciences 14:301–310. doi: 10.5194/bg-14-301-2017
Endoh T (2004) Historical review of reclamation works in the
Tokyo Bay area. J. Geograph. 113:785–801. (in
Japanese, with English abstract)
Falconer IR, Humpage AR (2005) Health risk
assessment of cyanobacterial (blue-green algal) toxins in drinking water. Int.
J. Environ. Res. Public Health 2:43–50. doi:10.3390/ijerph2005010043
Falkowski PG (2002) The ocean’s invisible
forest. Sci. Am. 287:54–61. doi: 10.1038/scientificamerican0802-54
Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls
and feedbacks on ocean primary production. Science 281:200–206. doi: 10.1126/science.281.5374.200
Feehan CJ, Grace SP, Narvaez CA (2019) Ecological
feedbacks stabilize a turf-dominated ecosystem at the southern extent of kelp
forests in the Northwest Atlantic. Sci. Rep. 9:7078. doi: 10.1038/s41598-019-43536-5
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary
production of the biosphere: Integrating terrestrial and oceanic components.
Science 281:237–240. doi:
10.1126/science.281.5374.237
Filbee-Dexter K, Wernberg T (2018) Rise of turfs:
A new battlefront for globally declining kelp forests. BioScience 68:64–76.
doi:10.1093/biosci/bix147
Fleming LE, Kirkpatrick B, Backer LC, Walsh CJ,
Nierenberg K, et al. (2011) Review of Florida red tide and human health effects. Harmful Algae 10:224–233. doi:10.1016/j.hal.2010.08.006
Friess DA, Rogers K, Lovelock CE, Krauss KW, Hamilton SE, et al. (2019) The
state of the world's mangrove forests: Past, present, and future. Annu. Rev. Environ.
Resour. 44:89–115. doi: 10.1146/annurev-environ-101718-033302
Frölicher TL, Laufkötter C (2018). Emerging risks from marine heat
waves. Nat. Commun. 9:650. doi: 10.1038/s41467-018-03163-6
Garibaldi L, Limongelli L (2002) Trends in oceanic captures and
clustering of Large Marine Ecosystems: two studies based on the FAO capture
database. FAO Fisheries Technical Paper. No. 435, FAO, Rome.
Glibert PM, Heil C, Rudnick DT, Madden CJ, Boyer JN, Kelly SP
(2009) Florida Bay: Water quality status and trends, historic and emerging
algal bloom problems. Contributions in Marine Science 38: 5–17.
Gobler CJ, Berry DL, Dyhrman ST, Wilhelm SW, Salamov A, et al. (2011) Niche of harmful alga Aureococcus anophagefferens revealed through
ecogenomics. Proc. Natl. Acad. Sci. U.S. A. 108:4352–4357. doi: 10.1073/pnas.1016106108
Go J, Nagai K, Segawa S, Honjo T (2016) M-ortality and impact on
life activity of Akoya pearl oysters caused by dinoflagellate Karenia
mikimotoi. J. Japanese society of Fish. Sci. 82:737–742. doi: 10.2331/suisan.15-00073
(in Japanese with English abstract)
Goes JI, Tian H, do Rosário Gomes H, Anderson OR, Al-Hashmi K, et al. (2020) Ecosystem state change in the Arabian Sea fuelled by the
recent loss of snow over the Himalayan-Tibetan Plateau region. Sci. Rep. 10:7422. doi: 10.1038/s41598-020-64360-2
Hallegraeff GM (2003) Harmful algal blooms: a global overview. In:
Hallegraeff, GM, Anderson DM, Cembella, AD (eds.) Manual on Harmful Marine Microalgae.
Monographs on Oceanographic Methodology, 11, 2nd edn. UNESCO Publishing, Paris,
pp. 25–49.
Heisler J, Glibert P, Burkholder J, Anderson DM,
Cochlan W, et al. (2008) Eutrophication and harmful algal blooms: A scientific consensus.
Harmful algae 8:3–13. doi: 10.1016/j.hal.2008.08.006
Hokkaido government Japan (2021) https://www.pref.hokkaido.lg.jp/sr/ssk/akashio_info.html (in Japanese, last access: 21 April 2022)
Hoyos CD, Agudelo PA, Webster PJ, Curry JA (2006) Deconvolution of
the factors contributing to the increase in global hurricane intensity. Science 312: 94–97. doi: 10.1126/science.1123560
Howarth RW, Sharpley A, Walker D (2002) Sources of
nutrient pollution to coastal waters in the United States: Implications for
achieving coastal water quality goals. Estuaries 25:656–676. doi: 10.1007/BF02804898
Huang B, Liang Y, Pan H, Xie L, Jiang T, Jiang T (2020) Hemolytic
and cytotoxic activity from cultures of Aureococcus anophagefferens —a causative species of
brown tides in the north-western Bohai Sea, China. Chemosphere 247:125819 doi: 10.1016/j.chemosphere.2020.125819
Huisman J., Codd GA, Paerl HW, Ibelings BW,
Verspagen JMH, Visser PM (2018) Cyanobacterial blooms. Nat. Rev.
Microbiol. 16:471–483. doi: 10.1038/s41579-018-0040-1
Humborg C, Ittekkot V, Cociasu A, Bodungen Bv (1997) Effect of
Danube River dam on Black Sea biogeochemistry and ecosystem structure. Nature 386:385–388. doi: 10.1038/386385a0
Ishikawa K, Kumagai M, Vincent WF, Tsujimura S, Nakahara H (2002) Transport
and accumulation of bloom-forming cyanobacteria in a large, mid-latitude lake:
the gyre-Microcystis hypothesis. Limnology 3:87–96. doi: 10.1007/s102010200010
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, et al.
(2001) Historical overfishing and the recent collapse of coastal ecosystems.
Science 293, 629–637. doi:10.1126/science.1059199
Jones BL, Unsworth RKF (2016) The
perilous state of seagrass in the British Isles. R. Soc. open sci.3:150596. doi:
10.1098/rsos.150596
Kahru M, Elmgren R, Kaiser J, Wasmund N, Savchuk O (2020) Cyanobacterial
blooms in the Baltic Sea: Correlations with environmental factors. Harmful
Algae 92:101739. doi: 10.1016/j.hal.2019.101739
Kerr RA (2006) Global warming may be homing in on Atlantic
hurricanes. Science 314:910–911. doi: 10.1126/science.314.5801.910
Kim CS, Lee SG, Lee CK, Kim HG, Jung J (1999) Reactive oxygen species
as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium
polykrikoides. J. Plankton Res. 21:2105–2115. doi: 10.1093/plankt/21.11.2105
Kuma K, Matsunaga K (1995) Availability of colloidal ferric oxides
to coastal marine phytoplankton. Mar. Biol. 122:1–11. doi: 10.1007/BF00349272
Li X, Yan T, Yu R, Zhou M (2019) A review of karenia mikimotoi:
Bloom events, physiology, toxicity and toxic mechanism. Harmful Algae 90:101702.
doi: 10.1016/j.hal.2019.101702
López-Cortés DJ, Núñez-Vázquez EJ, Dorantes-Aranda
JJ, Band-Schmidt CJ, Hernández-Sandoval FE, et al. (2019) The state of knowledge
of harmful algal blooms of Margalefidinium polykrikoides (a.k.a. Cochlodinium
polykrikoides) in Latin America. Front. Mar. Sci. 6:463. doi:
10.3389/fmars.2019.00463
Lotze HK, Lenihan HS, Bourque
BJ, Bradbury RH, Cooke RG, et al. (2006) Depletion, degradation, and recovery potential
of estuaries and coastal seas. Science
312:1806–1809. doi: 10.1126/science.1128035
Lovelock CE, Ball MC, Martin KC, Feller IC (2009) Nutrient enrichment increases mortality
of mangroves. PLoS One 4:e5600. doi:10.1371/journal.pone.0005600
Mann KH (1973) Seaweeds: Their
productivity and strategy for growth. Science 182: 975–981. doi: 10.1126/science.182.4116.975
Mardones JI, Norambuena L, Paredes J,
Fuenzalida G, Dorantes-Aranda JJ, et al. (2020) Unraveling the Karenia
selliformis complex with the description of a non-gymnodimine producing
Patagonian phylotype. Harmful Algae. 98:101892. doi: 10.1016/j.hal.2020.101892
Martin JH, Fitzwater SE (1988) Iron
deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature
331:341–343. doi: 10.1038/331341a0
Matsunaga K, Kawaguchi T, Suzuki Y, Nigi
G (1999) The role of terrestrial humic substances on the shift of kelp
community to crustose coralline algae community of the southern Hokkaido Island
in the Japan Sea. J. Exp. Mar. Biol. Ecol. 241:193–205. doi: 10.1016/S0022-0981(99)00077-5
Milliman JD (1997) Blessed dams or damned dams? Nature 386:325–327. doi: 10.1038/386325a0
Moyle PB, Cech JJ Jr. (2004) Fishes: An Introduction to Ichthyology,
5th edn. Pearson Benjamin Cummings, San Francisco.
NOAA (2021) Gulf of Mexico/Florida: Harmful algal blooms. https://oceanservice.noaa.gov/hazards/hab/gulf-mexico.html (last
access: 24 April 2022)
Nozawa A, Tsuji K, Ishida H (2003) Implication of brevetoxin B1
and PbTx-3 in neurotoxic shellfish poisoning in New Zealand by isolation and
quantitative determination with liquid chromatography-tandem mass spectrometry.
Toxicon 42:91–103. doi: 10.1016/s0041-0101(03)00123-5.
Odum EP (1971) Fundamentals of Ecology, 3rd edn. W. B.
Saunders Co., Philadelphia.
Okuma T (1981) Historical Review of the Relation between
Flood-Controls and Flood-Disasters in the Tone River Basin. Tokyo
University Press, Tokyo. (ISBN: 4-13-066053-5, in Japanese)
Oliver ECJ, Donat MG, Burrows MT, Moore PJ, Smale DA,
et al. (2018). Longer and more frequent marine heatwaves over the past century.
Nat. Commun. 9:1324. doi: 10.1038/s41467-018-03732-9
Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, et al. (2006) A global crisis for seagrass
ecosystems. Bioscience 56:987–996. doi: 10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2
Pauly D, Christensen V (1995) Primary production required to
sustain global fisheries. Nature 374:255–257. doi: 10.1038/374255a0
Pauly D, Christensen V, Guénette S, Pitcher TJ,
Sumaila UR, Walters CJ, Watson R, Zeller D (2002) Towards sustainability in
world fisheries. Nature 418:689–695. doi:10.1038/natue01017
Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58. doi: 10.1126/science.1155398
Pierce RH, Henry MS (2008) Harmful algal toxins of the Florida
red tide (Karenia brevis): natural chemical stressors in South Florida
coastal ecosystems. Ecotoxicology 17:623–631. doi: 10.1007/s10646-008-0241-x
Raven JA, Falkowski PG (1999) Oceanic sinks
for atmospheric CO2. Plant
Cell Environ. 22:741–755. doi: 10.1046/j.1365-3040.1999.00419.x
Ryan JP, Kudela RM, Birch JM, Blum M, Bowers HA, et al. (2017)
Causality of an extreme harmful algal bloom in Monterey Bay, California, during
the 2014–2016 northeast Pacific warm anomaly. Geophys. Res. Lett. 44:5571–5579. doi: 10.1002/2017GL072637
Sansom G (1963) A History of Japan: 1615–1867. Stanford University Press, Stanford, California.
Schirrmeister BE, Gugger M, Donoghue PCJ (2015)
Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils.
Palaeontology. 58:769–785. doi: 10.1111/pala.12178
Scholin CA, Gulland F, Doucette GJ, Benson S, Busman
M, et al. (2000) Mortality of sea lions along the central California coast
linked to a toxic diatom bloom. Nature 403:80–84. doi: 10.1038/47481
Sekula-Wood E, Schnetzer A, Benitez-Nelson CR, Anderson
C, Berelson WM, et al. (2009) Rapid downward transport of the
neurotoxin domoic acid in coastal waters. Nature Geosci. 2:272–275. doi: 10.1038/ngeo472
Shiklomanov LA (1993) World freshwater resources. In Gleick, PH
(ed.) Water in Crisis: A Guide to World's Freshwater Resources, Oxford
University Press, New York, pp. 13–24.
Simon N, Cras A-L, Foulon E, Lemée R (2009) Diversity and
evolution of marine phytoplankton. C. R. Biol. 332:159–170. doi: 10.1016/j.crvi.2008.09.009
Smale DA, Wernberg T, Oliver ECJ, Thomsen M, Harvey
BP, et al. (2019) Marine heatwaves threaten global biodiversity and the provision
of ecosystem services. Nat. Clim. Chang. 9:306–312. doi: 10.1038/ s41558-019-0412-1
Smetacek V (1998) Diatoms and the silicate factor. Nature 391:224–225. doi: 10.1038/34528
Spatharis S, Skliris N, Meziti A, Ar. Kormas K (2012) First
record of a Trichodesmium erythraeum bloom in the Mediterranean Sea. Can.
J. Fish. Aquat. Sci. 69:1444–1455. doi: 10.1139/f2012-020
Stal LJ, Albertano P, Bergman B, von Bröckel K, Gallon JR,
et al. (2003) BASIC: Baltic Sea cyanobacteria. An investigation of the
structure and dynamics of water blooms of cyanobacteria in the Baltic Sea—responses to a
changing environment. Cont. Shelf Res. 23:1695–1714. doi: 10.1016/j.csr.2003.06.001.
Steffen MM, B. Belisle BS, Watson SB, Boyer GL, Wilhelm SW (2014) Status,
causes and controls of cyanobacterial blooms in Lake Erie. J. Great Lakes Res. 40:215–225. doi: 10.1016/j.jglr.2013.12.012
Stramma L, Johnson GC, Sprintall J, Mohrholz V (2008) Expanding
oxygen-minimum zones in the tropical oceans. Science. 320:655–658. doi: 10.1126/science.1153847
Tajima K (2007) The marketing of
urban human waste in the early modern Edo/Tokyo metropolitan area. Environnement
Urbain/Urban Environment 1:a-13–a-30.
Takahashi T, Umehara A, Tsutsumi H (2014) Diffusion of
microcystins (cyanobacteria hepatotoxins) from the reservoir of Isahaya Bay,
Japan, into the marine and surrounding ecosystems as a result of large-scale
drainage. Mar. Pollut. Bull. 89:250–258. doi: 10.1016/j.marpolbul.2014.09.052
Tatters AO, Muhlstein HI, Tomas CR (2010) The hemolytic activity
of Karenia selliformis and two clones of Karenia brevis throughout
a growth cycle. J. Appl. Phycol. 22:435–442.
doi:10.1007/s10811-009-9476-z
Tilman D, Fargione J, Wolff B, D'Antonio C, Dobson A, et al.
(2001) Forecasting agriculturally driven global environmental change. Science.
13:281–284. doi: 10.1126/science.1057544
Toseland A, Daines SJ, Clark JR, Kirkham A, Strauss J, et al.
(2013) The impact of temperature on marine phytoplankton resource allocation
and metabolism. Nat. Clim. Chang. 3:979–984. doi: 10.1038/nclimate1989
Tréguer P, Bowler C,
Moriceau B, Dutkiewicz S, Gehlen M,
et al. (2018) Influence of diatom diversity on the ocean biological carbon pump. Nature Geosci, 11:27–37. doi: 10.1038/s41561-017-0028-x
Trainer VL, Bates SS, Lundholm N, Thessen AE, Cochlan WP, Adams NG,
Trick CG (2012) Pseudo-nitzschia physiological ecology, phylogeny,
toxicity, monitoring and impacts on ecosystem health. Harmful Algae, 14:271–300. doi:10.1016/j.hal.2011.10.025
Trenberth K (2005) Uncertainty in hurricanes and global warming. Science
308: 1753–1754. doi: 10.1126/science.1112551
Tsikoti C, Genitsaris S (2021) Review of Harmful Algal Blooms in the
Coastal Mediterranean Sea, with a Focus on Greek Waters. Diversity 13:396. doi:
10.3390/d13080396
Turkoglu M (2013) Red tides of the dinoflagellate Noctiluca
scintillans associated with eutrophication in the Sea of Marmara (the
Dardanelles, Turkey). Oceanologia 55:709–732. doi: 10.5697/oc.55-3.709
Unsworth RKF, Collier CJ, Waycott M, McKenzie LJ,
Cullen-Unsworth LC (2015) A framework for the resilience of seagrass
ecosystems. Mar. Pollut. Bull. 100:34–46. doi:10.1016/j.marpolbul.2015.08.016
Unsworth RKF, Nordlund LM, Cullen-Unsworth LC (2018)
Seagrass meadows support global fisheries production. Conserv. Lett. 12:e12566. doi: 10.1111/conl.12566
Uspensky M (2003) Hiroshige: One Hundred Views of Edo.
Sirocco, London.
Valiela I, Bowen JL, York JK (2001) Mangrove forests:
One of the world's threatened major tropical environments. BioScience 51:807–815. doi: 10.1641/0006-3568(2001)051[0807:MFOOTW]2.0.CO;2
van Puijenbroek PJTM, Beusen AHW,
Bouwman AF (2019) Global nitrogen and phosphorus in urban waste water based on
the Shared Socio-economic pathways. J. Environ. Manage. 231:446–456. doi:
10.1016/j.jenvman.2018.10.048
Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, et al. (2009)
Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc.
Natl. Acad. Sci. U.S.A. 106:12377–12381. doi:10.1073/pnas.0905620106
Whittaker RH, Likens GE (1973) Primary production: The biosphere and man. Hum. Ecol. 1:357–369. doi: 10.1007/BF01536732
Zhang Q, Qiu L, Yu R, Kong F, Wang Y, et al. (2012) Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China. Harmful Algae 19:117–124. doi: 10.1016/j.hal.2012.06.007