26. Stoichiometric Analysis of Pelagic Ecosystems: The Biogeochemistry of Planktonic Food Webs
391
The flexibility of phytoplankton lies at both the
intraspecific and interspecific levels. When a given
species is grown under chemostat conditions in
which growth rate, light, temperature, and nutrient
supply ratios are altered, the chemical composition
of cellular biomass changes dramatically in predictable ways. A very large literature on these responses exists; I highlight major findings here.
First, algae growing at differing rates in chemostats (i.e., growing at various degrees of nutrient
limitation) generally have strongly altered elemental composition. More specifically, if algal growth
rate is limited by a single nutrient X, then cellular
carbon (C)JX ratio increases with decreasing
growth rate (Goldman et al. 1979; Healey and
Hendzel 1980) (Fig. 26.2A). Second, algae "are
what they eat" in terms of macronutrient supply.
That is, at any given growth rate, when the
nitrogen/phosphorus (NIP) ratio of the inflow medium is changed, cellular NIP responds in parallel
(due to lUXUry accumulation of the nonlimiting nutrient), so that high supply NIP ratios generate algal biomass with high NIP ratio and vice versa
(Rbee 1978). Third, algae "are what they eat" in
terms of their response to light intensity as well
(Fig. 26.2B). That is, at a fixed growth rate under
nutrient limitation, increased light intensity raises
the CJX ratio (where X is the limiting nutrient)
(Healey 1985; Rhee and Gotham 1981; Smith
1983). Thus, algal biomass also comes to reflect
the balance of supply of light and limiting nutrient.
Finally, these physiological responses vary from
species to species according to the competitive
abilities of individual taxa as algal species differ
in terms of nearly all of the physiological parameters that determine the growth response to resource supply (Tilman 1982; Andersen 1997) (Fig.
26.2C). For example, the Nand P composition at
zero growth rate (the so-called "optimal NIP ratio"
or NIP opt) (Tilman 1982) differs considerably
among species, with blue-green algae having low
NlP opt (and thus being good competitors for N but
weak competitors for P) while green algae and diatoms have high NlP opt (and thus compete well
when P is scarce compared with N).
From the work just reviewed we see that algal
elemental composition is a function of the severity
of nutrient limitation (in terms of decreased growth
rate), the identity of the limiting nutrient, the nutrient composition of the supply, ambient light intensity, and algal species identity. Thus, the key
message from the literature on the nutritional physiology of algae is that we should expect to find
considerable variation in the elemental composition
of algal biomass at the base of pelagic food webs.
Indeed this is what we see when we look at
C/nutrient ratios in suspended organic matter in
lakes and oceans (Fig. 26.3) (Elser and Hassett
1994; Sterner and Hessen 1994). From an ecosystem perspective, what this means is that primary
production is a highly heterogeneous process in
biogeochemical terms. Additional data supporting
this connection have recently been analyzed by
Sterner et al. (1997) who documented strong variation in the CIP of suspended organic matter at the
base of pelagic food webs in Canadian Shield lakes.
Specifically, they found that small, sheltered lakes
had very high CIP ratios in particulate matter, while
large, well-mixed lakes (including Lake Superior)
had particulate matter with lower, more balanced
CIP composition. Sterner and colleagues propose
an explanation for these patterns, the "light/nutrient
hypothesis," arguing that hydrodynamic conditions
change dramatically as lakes increase in surface
area, modifying the light and P supply balance experienced by algae in the surface mixed layer and
thus the CIP ratio of organic matter production.
They also describe a suite of ecological consequences of variation in the stoichiometry of autotroph production, including effects on the strength
of the microbial food web, the species composition
of the zooplankton (due to food quality effects discussed below), and the strength of "top down" effects in the food web. Experimental support for the
effect of light/nutrient balance in regulating algal
CIP and grazer success has been produced (Urabe
and Sterner 1996; Sterner et al. 1998). These findings suggest that to better understand physicalbiological coupling in the pelagic zone we need to
move away from our tendency to consider energy
flow and nutrient cycling as distinct topics. Energy
and nutrients are linked in intimate and critical
ways, and a future challenge will be to develop
frameworks that integrate both energy and matter
in a single system.
Terrestrial ecosystem scientists may recognize a
close parallel between the CIP ecophysiology of
phytoplankton just described and the influential
concepts of "nutrient use efficiency" (Vitousek
1982) and "nutrient productivity" (Agren 1988)
391
The flexibility of phytoplankton lies at both the
intraspecific and interspecific levels. When a given
species is grown under chemostat conditions in
which growth rate, light, temperature, and nutrient
supply ratios are altered, the chemical composition
of cellular biomass changes dramatically in predictable ways. A very large literature on these responses exists; I highlight major findings here.
First, algae growing at differing rates in chemostats (i.e., growing at various degrees of nutrient
limitation) generally have strongly altered elemental composition. More specifically, if algal growth
rate is limited by a single nutrient X, then cellular
carbon (C)JX ratio increases with decreasing
growth rate (Goldman et al. 1979; Healey and
Hendzel 1980) (Fig. 26.2A). Second, algae "are
what they eat" in terms of macronutrient supply.
That is, at any given growth rate, when the
nitrogen/phosphorus (NIP) ratio of the inflow medium is changed, cellular NIP responds in parallel
(due to lUXUry accumulation of the nonlimiting nutrient), so that high supply NIP ratios generate algal biomass with high NIP ratio and vice versa
(Rbee 1978). Third, algae "are what they eat" in
terms of their response to light intensity as well
(Fig. 26.2B). That is, at a fixed growth rate under
nutrient limitation, increased light intensity raises
the CJX ratio (where X is the limiting nutrient)
(Healey 1985; Rhee and Gotham 1981; Smith
1983). Thus, algal biomass also comes to reflect
the balance of supply of light and limiting nutrient.
Finally, these physiological responses vary from
species to species according to the competitive
abilities of individual taxa as algal species differ
in terms of nearly all of the physiological parameters that determine the growth response to resource supply (Tilman 1982; Andersen 1997) (Fig.
26.2C). For example, the Nand P composition at
zero growth rate (the so-called "optimal NIP ratio"
or NIP opt) (Tilman 1982) differs considerably
among species, with blue-green algae having low
NlP opt (and thus being good competitors for N but
weak competitors for P) while green algae and diatoms have high NlP opt (and thus compete well
when P is scarce compared with N).
From the work just reviewed we see that algal
elemental composition is a function of the severity
of nutrient limitation (in terms of decreased growth
rate), the identity of the limiting nutrient, the nutrient composition of the supply, ambient light intensity, and algal species identity. Thus, the key
message from the literature on the nutritional physiology of algae is that we should expect to find
considerable variation in the elemental composition
of algal biomass at the base of pelagic food webs.
Indeed this is what we see when we look at
C/nutrient ratios in suspended organic matter in
lakes and oceans (Fig. 26.3) (Elser and Hassett
1994; Sterner and Hessen 1994). From an ecosystem perspective, what this means is that primary
production is a highly heterogeneous process in
biogeochemical terms. Additional data supporting
this connection have recently been analyzed by
Sterner et al. (1997) who documented strong variation in the CIP of suspended organic matter at the
base of pelagic food webs in Canadian Shield lakes.
Specifically, they found that small, sheltered lakes
had very high CIP ratios in particulate matter, while
large, well-mixed lakes (including Lake Superior)
had particulate matter with lower, more balanced
CIP composition. Sterner and colleagues propose
an explanation for these patterns, the "light/nutrient
hypothesis," arguing that hydrodynamic conditions
change dramatically as lakes increase in surface
area, modifying the light and P supply balance experienced by algae in the surface mixed layer and
thus the CIP ratio of organic matter production.
They also describe a suite of ecological consequences of variation in the stoichiometry of autotroph production, including effects on the strength
of the microbial food web, the species composition
of the zooplankton (due to food quality effects discussed below), and the strength of "top down" effects in the food web. Experimental support for the
effect of light/nutrient balance in regulating algal
CIP and grazer success has been produced (Urabe
and Sterner 1996; Sterner et al. 1998). These findings suggest that to better understand physicalbiological coupling in the pelagic zone we need to
move away from our tendency to consider energy
flow and nutrient cycling as distinct topics. Energy
and nutrients are linked in intimate and critical
ways, and a future challenge will be to develop
frameworks that integrate both energy and matter
in a single system.
Terrestrial ecosystem scientists may recognize a
close parallel between the CIP ecophysiology of
phytoplankton just described and the influential
concepts of "nutrient use efficiency" (Vitousek
1982) and "nutrient productivity" (Agren 1988)