burrows, providing them with water, shelter, and protection from predators. Polychaetes and bivalves are invertebrates that are able to respire anaerobically, and during this
period, the metabolic rate is usually greatly depressed.
Hypoxia and anaerobic metabolism
Survival in low-oxygen conditions is an important adaptation for estuarine organisms, where the tolerance is
affected by numerous factors, including temperature, light
intensity, body weight, pH, and feeding conditions. For
example, in the shrimp Litopenaeus vannamei, which
lives at 1–2 to 40 psu, tolerance to hypoxia is greatest
when it has been cultured at the optimal salinity for growth
(Zhang et al., 2006).
Many animals can simultaneously respire both aerobically and anaerobically, but the ability to respire anaerobically is critical for many estuarine polychaete worms and
bivalves. As in the case of aerobic respiration, anaerobic
respiration depends on having a suitable substrate to provide energy, but it has a lower yield and produces end
products which need to be stored or excreted later. While
some animals, fish, and crustaceans use glycogen for
energy production, this results in the accumulation of large
amounts of lactate. Many brackish-water organisms use an
alternative anaerobic pathway, incorporating amino acids,
such as arginine, which yields similar amounts of energy
but has a different end product, and octopine, which may
interfere less with particular enzyme systems. Bivalve
mollusks and gastropods are particularly resistant to
anoxia because they are able to establish homeostasis once
oxygen becomes available, and they can avoid the damaging effects of rapidly increasing oxygen radicals, which
lead to oxidative stress (Freire et al., 2011a). The antioxidant defenses of mollusks include the production of
enzymes (e.g., superoxidase dismutase and glutathione).
During anoxia, increased activities of catalase and glutathione S-transferase (GST) have been recorded in the gills
of estuarine crab Chasmagnathus (Neohelice) granulata.
It is suggested that species from more challenging habitats, for example, those stressed by temperature, salinity,
and low oxygen, show higher activities of stress indicators
such as heat-shock proteins, blood cortisol levels, and
antioxidant levels (Freire et al., 2011a; Freire et al.,
2011b). Both increased and decreased salinities affected
expression/activities of enzymes of the antioxidant system. In a comparison of two closely related crabs which
have different distributions, the species from the inner
estuary was expected to have high levels of antioxidant
enzymes compared with crabs from the more stable
marine environment. This was found to be true; the more
euryhaline species had greater activity of antioxidative
enzymes, the less euryhaline species exhibited activation
of these enzymes when exposed to air or hypersalinity.
Growth and energetics
For many organisms, the growth patterns are controlled by
both internal and environmental factors including salinity
which can affect reproduction and the success of larval
stages (Pechenic and Kerr, 2000; Pechenic et al., 2003).
Growth rate is highly dependent on the energy budget,
and changes in the growth rate as a result of salinity flux
are potentially affected by the standard or basal metabolic
rate, quantity and quality of the food supply, food conversion, and perhaps hormonal stimulation. For estuarine
clams, growth is best at intermediate salinities and often
reduced at low salinities (Carmichael et al., 2004;
Marsden, 2004). For flatfish (flounders), there is an optimal salinity for early development and larval growth, but
this is species specific (Smith et al., 1999; Specker et al.,
1999). There is considerable evidence showing that salinity influences growth in fish (Boeuf and Payan, 2001), and
optimal growth occurs at intermediate salinities
(8–20 psu). Sometimes this is the result of lowered standard metabolic rate, but it may not always be the case,
because growth rate may also be affected by food intake,
swimming performance, and activity patterns. In salmonids, there is hormonal control of salmon smoltification
involving both osmoregulation and growth. It was thought
that between 20 % and 50 % of the energy budget in fish
was allocated toward osmoregulation, but other studies
suggest it may be considerably lower ($10 % in isolated
gills of cutthroat trout) (Morgan and Iwama, 1999). This
remains a subject of ongoing debate.
Behavioral mechanisms and biological rhythms
Behavioral mechanisms allow mobile estuarine organisms
to evade the stresses associated with shallow water environments; shrimp and crabs typically move away from
dangerous hypoxic conditions. Burrowing in soft sediments is also a key adaptation, solving all the problems
associated with osmotic, respiratory, and thermal stress
at low tide. Many fish have seasonal patterns of development and migrate in and out of estuaries. Some crabs enter
estuaries at high tide to exploit mudflat habitats, while
avoiding avian predators and stresses associated with
aerial exposure. The reproductive strategies of estuarine
invertebrates including polychaetes are often more complex than open-coastal species, and larval release of
benthic decapod crustaceans occurs according to lunar,
light–dark, or tidal cycles. Spawning is usually synchronized with particular tidal conditions and larval behavior
(including vertical migrations) to ensure that juveniles
move back into estuaries and settle in a habitat which provides good conditions for growth (Naylor, 1976).
In the past, considerable research has been conducted to
assess the mechanisms controlling rhythmic behavior of
invertebrates. Crabs have been studied in detail, and
research suggests that the behavior is controlled by
a combination of external and internal (endogenous) factors, involving an internal clock (Naylor, 2001). Estuarine
crabs held in constant conditions in the laboratory in the
dark continue to display locomotor rhythms correlated
with the tides and the moon with a periodicity of
12.4 h which occurs twice in each lunar day (24.8 h).
488
PHYSIOLOGICAL MECHANISMS
period, the metabolic rate is usually greatly depressed.
Hypoxia and anaerobic metabolism
Survival in low-oxygen conditions is an important adaptation for estuarine organisms, where the tolerance is
affected by numerous factors, including temperature, light
intensity, body weight, pH, and feeding conditions. For
example, in the shrimp Litopenaeus vannamei, which
lives at 1–2 to 40 psu, tolerance to hypoxia is greatest
when it has been cultured at the optimal salinity for growth
(Zhang et al., 2006).
Many animals can simultaneously respire both aerobically and anaerobically, but the ability to respire anaerobically is critical for many estuarine polychaete worms and
bivalves. As in the case of aerobic respiration, anaerobic
respiration depends on having a suitable substrate to provide energy, but it has a lower yield and produces end
products which need to be stored or excreted later. While
some animals, fish, and crustaceans use glycogen for
energy production, this results in the accumulation of large
amounts of lactate. Many brackish-water organisms use an
alternative anaerobic pathway, incorporating amino acids,
such as arginine, which yields similar amounts of energy
but has a different end product, and octopine, which may
interfere less with particular enzyme systems. Bivalve
mollusks and gastropods are particularly resistant to
anoxia because they are able to establish homeostasis once
oxygen becomes available, and they can avoid the damaging effects of rapidly increasing oxygen radicals, which
lead to oxidative stress (Freire et al., 2011a). The antioxidant defenses of mollusks include the production of
enzymes (e.g., superoxidase dismutase and glutathione).
During anoxia, increased activities of catalase and glutathione S-transferase (GST) have been recorded in the gills
of estuarine crab Chasmagnathus (Neohelice) granulata.
It is suggested that species from more challenging habitats, for example, those stressed by temperature, salinity,
and low oxygen, show higher activities of stress indicators
such as heat-shock proteins, blood cortisol levels, and
antioxidant levels (Freire et al., 2011a; Freire et al.,
2011b). Both increased and decreased salinities affected
expression/activities of enzymes of the antioxidant system. In a comparison of two closely related crabs which
have different distributions, the species from the inner
estuary was expected to have high levels of antioxidant
enzymes compared with crabs from the more stable
marine environment. This was found to be true; the more
euryhaline species had greater activity of antioxidative
enzymes, the less euryhaline species exhibited activation
of these enzymes when exposed to air or hypersalinity.
Growth and energetics
For many organisms, the growth patterns are controlled by
both internal and environmental factors including salinity
which can affect reproduction and the success of larval
stages (Pechenic and Kerr, 2000; Pechenic et al., 2003).
Growth rate is highly dependent on the energy budget,
and changes in the growth rate as a result of salinity flux
are potentially affected by the standard or basal metabolic
rate, quantity and quality of the food supply, food conversion, and perhaps hormonal stimulation. For estuarine
clams, growth is best at intermediate salinities and often
reduced at low salinities (Carmichael et al., 2004;
Marsden, 2004). For flatfish (flounders), there is an optimal salinity for early development and larval growth, but
this is species specific (Smith et al., 1999; Specker et al.,
1999). There is considerable evidence showing that salinity influences growth in fish (Boeuf and Payan, 2001), and
optimal growth occurs at intermediate salinities
(8–20 psu). Sometimes this is the result of lowered standard metabolic rate, but it may not always be the case,
because growth rate may also be affected by food intake,
swimming performance, and activity patterns. In salmonids, there is hormonal control of salmon smoltification
involving both osmoregulation and growth. It was thought
that between 20 % and 50 % of the energy budget in fish
was allocated toward osmoregulation, but other studies
suggest it may be considerably lower ($10 % in isolated
gills of cutthroat trout) (Morgan and Iwama, 1999). This
remains a subject of ongoing debate.
Behavioral mechanisms and biological rhythms
Behavioral mechanisms allow mobile estuarine organisms
to evade the stresses associated with shallow water environments; shrimp and crabs typically move away from
dangerous hypoxic conditions. Burrowing in soft sediments is also a key adaptation, solving all the problems
associated with osmotic, respiratory, and thermal stress
at low tide. Many fish have seasonal patterns of development and migrate in and out of estuaries. Some crabs enter
estuaries at high tide to exploit mudflat habitats, while
avoiding avian predators and stresses associated with
aerial exposure. The reproductive strategies of estuarine
invertebrates including polychaetes are often more complex than open-coastal species, and larval release of
benthic decapod crustaceans occurs according to lunar,
light–dark, or tidal cycles. Spawning is usually synchronized with particular tidal conditions and larval behavior
(including vertical migrations) to ensure that juveniles
move back into estuaries and settle in a habitat which provides good conditions for growth (Naylor, 1976).
In the past, considerable research has been conducted to
assess the mechanisms controlling rhythmic behavior of
invertebrates. Crabs have been studied in detail, and
research suggests that the behavior is controlled by
a combination of external and internal (endogenous) factors, involving an internal clock (Naylor, 2001). Estuarine
crabs held in constant conditions in the laboratory in the
dark continue to display locomotor rhythms correlated
with the tides and the moon with a periodicity of
12.4 h which occurs twice in each lunar day (24.8 h).
488
PHYSIOLOGICAL MECHANISMS