Resilience in aquatic ecosystems - hysteresis, homeostasis, and ...

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Reynolds/ Aquatic Ecosystem Health and Management 5 (2002) 3–17
times) between instances of severe forcing and with
the more quiescent interludes that provide opportunities
for restructuring, hampers the progress of an
ecosystem towards energetic steady state. The deduction
is no more than a restatement of Connell’s (1978)
Intermediate Disturbance Hypothesis.
The effect of resources on community
assembly
The second main impediment to the achievement
by a developing ecosystem of its energy-determined
potential is the premature exhaustion of the supply of
one or other of the component elements. The effects
of nutrient sparsity are well-recognized in aquatic systems,
where sharp physical boundaries, across which
exchange rates are defined or measurable, together
with a well-developed understanding of the nutrient
chemistries and a suite of sensitive analytical techniques,
all contribute to the relative ease of determining
availability and demand. Moreover, the composition
of protoplasm is broadly similar among bacteria,
protists, plants and animals: to be able to assemble
biomass requires the delivery of up to twenty elements,
some of which are much harder to attain, relative
to requirement, than the others. For instance, this
consistent cell stoichiometry indicates that in order to
build as much as 50 g cell C m –2 requires the assimilation
of an average of 1.2 g P, 9 g N and 0.05 g
Fe m –2 . For various reasons (electrochemical binding
to oxides, chemical inertia, insolubility), natural
hydraulic exchanges are rarely able to maintain appropriate
fluxes of all three elements. The affinity of the
uptake mechanisms of the primary producers is usually
very well-developed, and able to reduce the
bioavailable sources to very low levels, indeed. In the
plankton, at least, if bioavailable nutrient can be
measured, primary production is not limited. Among
temperate freshwaters, phosphorus exhaustion is a
frequent limiting constraint, whereas nitrogen is generally
supposed to be relatively the scarcest in lakes of
tropical and arid regions, as well as in the coastal and
shelf waters of the sea. In the Pacific Ocean, where
concentrations of N and P are also habitually quite
low, experiments have nevertheless revealed that iron
maintains the critical limit (Martin and Fitzwater,
1988).
One or other of these nutrients then sets a maximum
carrying capacity on the system, which in terms
of active biomass, can be marked as an offset on the x
axis of Figure 1 in order to re-define the shape of the
exergy buffer (now reminiscent of the sail of a dhow
or, perhaps, a windsurfer; see Figure 3a). The new
boundary reduces the limits within which biomass
assembly occurs but leaves the supportable limit with
a margin of exergy. As is true of the other two margins,
proximity of the system coordinates to the
resource limit is indicative of strong selection for
appropriate adaptive traits. However, the identity of
the species to which any advantage may accrue will
depend on just which resource it is that is deficient.
Exhaustion of bioavailable silicon (which is not a
problem for most non-diatoms) would favour a different
outcome from exhaustion of bioavailable nitrogen
compounds (which is, supposedly, no bar to the
growth of dinitrogen-fixing Cyanobacteria). However,
for other resources, such as phosphorus, the requirement
is universal and the dependence upon an appropriate
source is common. The crucial property in
which planktonic algae vary is in their uptake affinity
for the resource at very low concentrations. In
essence, a high affinity permits one species to be able
to gain more of its immediate resource requirement
than its competitors, thereby permitting it to sustain
its growth for longer, to add to its own potential exergy
flux and, in all probability, to build a larger standing
population than its rivals. Crucially, this may also
mean an enhanced ability to recruit future populations
when suitable conditions return, because a relatively
greater number of propagules are poised to exploit the
next growth opportunity. So it is that dominant organisms
frequently match, and are indicative of, the habitats
in which they occur preferentially.
For examples of superior affinity, one need look no
further than the classic experiments of Tilman and
Kilham (1976) or of Rhee (1978). These revealed how
much “further” certain algal species perform than others
when low external nutrient concentrations obtain.
Interestingly, the adaptations tend to be nutrient-specific,
so that being able to operate on lower phosphorus
concentrations than can other species is in no
sense a guarantee of being able to work also at low
concentrations of, for example, silicon or nitrogen. In
fact, there is often an element of “trade-off ” with specialists
in, say, silicon uptake having a relatively weak
affinity for phosphorus, and vice versa. The key to
this behavior is presumably the number of ion-specific
acceptor sites per unit of biomass and the level to
which the internal transport and assimilation can fall
before the cell recognizes its own nutrient deficiency
(see Mann, 1995). In practical terms, the behavior is
revealed in the specific values of the vectors characterizing
the Michaelis-Menten description of uptake
dynamics. The higher is the value of maximum uptake