Download MANN, K. H. Production and use of detritus in various freshwater

Limnol. Oceanogr., 33(4, part 2), 1988, 9 IO-930
0 1988, by the American
Society of Limnology
and Oceanography,
Inc.
Production and use of detritus in various freshwater,
estuarine, and coastal rnarine ecosystems
K. H. Mann
Department
Dartmouth,
of Fisheries and Oceans, Marine
Nova Scotia B2Y 4A2
Ecology Laboratory,
Bedford
Institute
of Oceanography,
Abstract
In both freshwater and marine habitats, vascular marine plants arc little used by animals that
graze directly on them, because they have a relatively high content of indigestible fiber and a low
content of nitrogen. The chief emphasis of detritus research in the 1970s was to show how microorganisms progressively reduce the content of fiber and increase the content of nitrogren in vascular
plant detritus, rendering it nutritious for animals. Algal (seaweed, diatom, etc.) detritus starts with
a lower fiber content and a higher nitrogen content. Many animals can use it directly, and a very
short period of microbial colonization renders it highly nutritious. As a result, a high proportion
of the algal carbon originally produced passes into animals via detrital food webs, while a low
proportion of vascular plant carbon does so. Much more of the latter simply supports microbial
respiration.
In the 1980s it was shown, particularly for freshwater habitats, that the dissolved organic matter
(DOM) released by plants while living or in the early stages of decomposition readily precipitates
on surfaces and forms amorphous particulate matter with a low content of refractory material.
These particles are highly nutritious for animals and are used directly by freshwater fish such as
Sarotherodon (= Tifapia), which is commercially important, especially in Africa and South America.
It is suggested that the DOM pathway may be ecologically more significant than the POM (particulate organic matter) pathway and that processes analogous to those shown for lakes and rivers
probably occur in estuarine and coastal waters.
There is much circumstantial evidence to suggest that planktonic food webs based on DOM are
much more important than previously thought. The conversion of DOM to POM through the
“microbial
loop” and its utilization in higher trophic levels is a.n urgent topic for further study.
In most situations more energy and materials flow through detritus food webs than
through grazer food webs. Of the total primary production of a system, more is transmitted to other trophic levels from dead
decomposing plant tissue than from living
tissue consumed by a grazer. Nevertheless,
those who manage aquatic systems for high
productivity
of fish, shellfish, or other invertebrates will be interested not so much
in the total flow of energy and materials as
in those pathways leading directly to nutrition for species of interest. Hence, one
question addressed here is the extent to
which detritus pathways support the production of invertebrates and fish, and the
extent to which they lead mainly to the production of CO, in microbial respiration and
to the regeneration of nutrients.
Another question concerns the relative
importance of plant detritus derived from
vascular plants (salt marsh grasses, seagrasses, mangroves) and that derived from seaweeds and other algae. Historically,
great
emphasis has been placed on studying the
fate of vascular plant detritus, and the fate
of algal detritus is less well understood.
Finally, much more attention has been
paid to particulate organic matter (POM)
than to dissolved organic matter (DOM)
which may be released either from living
plants or from dead plants during the early
stages of decomposition. We shall see that
this emphasis may have been misplaced,
and that the detrital pathways that begin
with DOM may be ecologically more significant.
Nitrogen as a limiting factor
Very few aquatic macrophytes are extensively used by grazers (Teal 1962; Odum
and de la Cruz 1967; Mann 1972; Fisher
and Likens 1973; Dickinson
and Pugh
19’74). Leaves and stems die and decay and
supply large quantities of plant detritus to
the systems in which they occur. This is
particularly
true of plants growing in the
littoral zones of lakes and rivers, in freshwater and saltwater marshes, in seagrass and
seaweed beds, and in mangrove swamps. Tn
910
Detritus: Production and use
911
this material was fed to Capitella, they found
addition,
terrestrial
plants overhanging
streams make a major contribution
of dethat on a diet of marsh grass detritus Captritus to these systems. With the exception
itella obtained about a third of its nitrogen
of the algae, all of these plants tend to have ’ from the plant material; on seaweed detritus
a high content of fibrous material, such as it obtained ~80%.
There is other evidence that not all the
lignin or cellulose and a low content of nitrogen. Such material is of limited food valdigestible nitrogen in detritus is in the form
ue for animals, since the carbon is largely
of microbial protein. Bowen (1980) analyzed detritus from the littoral zone of lakes
indigestible and there is very little protein.
Nature’s solution to this dilemma is to
and found that protein accounted for less
than a third of the total nitrogen present.
invoke the aid of microbes, both fungi and
bacteria but particularly the latter. Many of The remainder was mainly in the form of
nonprotein amino acids present in the dead
them have the ability to digest cellulose and
particulate organic matter rather than the
other refractory carbon compounds. As time
microorganisms. He went on to show that
progresses, the detrital material is attacked
the fish Sarotherodon (=Tilapia) could use
by the microbes and broken into finer parthese amino acids very efficiently (see beticles making still more surface available
for colonization.
Refractory carbon comlow). Two workers in my own laboratory
pounds are processed to yield energy for
had previously drawn attention to the exmicrobial metabolism, while additional niistence of nonprotein nitrogen in detritus,
trogen for microbial protein is taken from
although no further investigations had been
the environment. As the ratio of microbial
made (Harrison and Mann 1975a; Robinbiomass to plant tissue increases, the detrison et al. 1982). Lee et al. (1980) found that
tal particles become more nutritious for inmicrobes accounted for only a minor part
vertebrates. Invertebrates readily digest the
of the relative increase in nitrogen observed
microbial component, allowing much of the
during decomposition of Spartina, and Rice
refractory plant tissue to pass through their
(1982) pointed out that during decompoguts. This process by which microbes make
sition detritus becomes richer in reactive
detrital carbon available to animals and play
phenolic and carbohydrate groups, which
an essential part in overcoming the nitrogen
may form condensation products with amideficiency of detrital food has been demno acids, yielding precursors to complex nionstrated many times in a variety of habitrogenous humic substances. These are liketats (Newell 1965; Odum and de la Cruz
ly to be indigestible to most detritivores.
1967; Mann 1972; Dickinson
and Pugh
Dissolved organic matter and the
1974; Fenchel and Jorgensen 1977; Pomeformation
of detrital aggregates
roy 1980). One of the most convincing demonstrations that the efficiency of transforWhen dead plant material begins to demation of plant detritus to animal tissue is compose, there is a rapid loss of soluble
proportional to the nitrogen content and inorganic matter (Kaushik and Hynes 1971;
versely proportional to the fibrous content
Wetzel and Manny 1972; Harrison and
was that of Tenore (1977, 198 1) who worked
and Fisher
Mann 1975a, b; McDowell
with laboratory cultures of the polychaete
1976). Living plants also produce dissolved
worm Capitella that were fed standard diets
organic matter in greater or lesser amounts
of different types of detritus (Fig. 1).
depending on such variables as nutrient
Recent work has shown that for some supply and light conditions (Sieburth 1969;
kinds of detritus, especially that from algae, Gallagher
et al. 1976; Fankboner
and
the animals can absorb substantial amounts
deBurgh 1977; Azam and Ammerman
of nitrogen directly from the plant material.
1984). As a result, there is an influx of DOM
Findlay and Tenore ( 1982) succeeded in
into all aquatic environments. A proportion
producing marsh grass detritus and seaweed of this is rapidly taken up by bacteria (which
detritus in which a 15N label had been inmay themselves be grazed and contribute
corporated into only the plant material, only
to invertebrate and vertebrate food chains),
the coating of microbes, and both. When
which also deposit organic matter in par-
Mann
912
MARSH
GRASS
2
EEL
GRASS
tt
F
MIXED
CEREAL
FUCUS
GRACILARIA
t
t
t
N
‘E 600
mg
Table 1. Survival and mean final weight of groups
of 10 tadpoles (Bz@ americanus) fed test diets for 6 d.
FOOD / DAY :
a
a
i 400
w
+
E
--
8
3 200
t?
a
F
o.I-
NITROGEN
IN FbOD
SOURCE
(% 1
Fig. 1. Production of the worm C’apiMia as a fimction of the nitrogen content of its food and the level
of ration (from Tenore 1977).
ticulate form, such as exoenzymes, mucus,
and the ropelike aggregates described by
Paerl(1978). Another fraction of the DOM
is converted to particulate form by physicochemical processes that occur on interfaces, e.g. on plant and on rock surfaces, on
sediment particles, at the surfaces of bubbles, and at the surface of any water body.
Detritus formed in this way reveals no cellular structure and may thus be clearly distinguished from plant detritus. Bowen (1984)
referred to the two types as amorphous and
morphous particulate organic matter (POM)
and has shown that the amorphous material
is often readily digestible by animals without the aid of microbes (Table 1). Camilleri
and Ribi ( 1986) showed that DOM released
by mangrove leaves can be converted to
flakes, which are used as food by copepods,
amphipods, isopods, and shrimps.
The eficiency of various
detrital pathways
There are five different pathways by which
the energy and materials of primary production may be transferred to invertebrates
and vertebrates in aquatic habitats, three of
which involve microbes as essential intermediaries (Fig. 2). The processes of fragmentation, colonization
by microbes, and
enrichment with nitrogen, often called aging
of detritus, proceeds more or less rapidly
according to the nature of the original plant
material and the environmental conditions.
During decay, microorganisms use the plant
detritus for their own metabolism. If the
interval between the onset of detritus for-
Test diet
DOM precipitated with FeCl,
DOM precipitated, no added
agent
DOM with bacterial suspension
Leached plant fragments
Control I (starved)
Control II (starved)
Cumulative survival
(tadpole
days)
Final
wt (mg)
38
17.2-t 1.23
58
28.3-+ 1.59
54
5
10
2
37.3k3.43
--
mation and consumption by an animal is
long, microbes convert a large proportion
of the plant material to CO*, in which case
the efficiency of transfer of energy and materials from plant to invertebrate will be very
low. By contrast, a trophic transfer in which
plant organic matter is assimilated directly
by invertebrates or fish may have a relatively high efficiency. In what follows, we
enquire about the efficiency of detrital utilization in a range of habitats and use this
information to try to assess the relative importance of detritus and grazer pathways in
supporting the productivity
of fish and
shellfish.
De&us in streams
IJpper reaches- There is no doubt that
the detritus pathway is dominant in tributaries of rivers originating in forested uplands. In Bear Brook, a small headwater
stream in the eastern United States (Fisher
and Likens 1973), almost all input of energy
and materials is from forest detritus. Trees
shade the stream and inhibit primary production in the streambed. New Hope Creek,
studied by Hall (1972) is more open, and
there is a significant product of periphyton
in the stream, but even there the input of
carbon from dead leaves from the trees was
twice as large as the carbon fixed by periplhyton.
Leaf packs provide habitats for aquatic
invertebrates that shred and collect leaves
and leaf fragments. Examples of shredders
are stonefly larvae and some kinds of caddis
fly larvae, while blackfly larvae and netspinning caddis larvae are collectors. Short
Detritus: Production and use
913
Animals
- Digest *
Morphous
Particles
Particulate
Detritus
(Morphous)
\
/
Dead
Plant
Tissue
Animals
Colonization
:;&I
/
%Zes
Microbes
\
/
Dissolved
Organic
Matter
Formation of
Amorphous
Particles
\
\
:;gE,
Precipitation
Animals
Digest
Amorphous
Particles
/
Fig. 2. Pathways of utilization
Discussion given in text.
of plant detritus.
and Maslin (1977) labeled leaves of a young
alder tree with 32P. When these were exposed as leaf packs in an artificial stream
along with various combinations of insect
larvae, Short and Maslin found that the
presence of the stonefly Pteronarcys as a
shredder increased the uptake of 32P by the
net-spinning
caddis Hydropsyche by 35100% and the uptake of the blackfly larva
Simulium by 600-700% (Fig. 3). This is a
direct demonstration both of the transfer of
detrital material into invertebrate food webs
and of the importance of shredder species
in preparing
the material
for collector
species.
Stream ecologists have also demonstrated
experimentally
the importance of DOM in
supporting the production of stream insects,
and hence of fish. Rounick and Winterbourn (1983) showed that DOM in stream
water will precipitate on stone surfaces, both
in the light and in the dark, to form a slime
layer which stream insects readily ingest. In
nature, the upper surfaces of stones have a
layer consisting of periphyton algae, the organic slime layer, and associated bacteria
and fungi, and it is clear that the removal
of this layer by browsing insects provides
surfaces on which precipitation
of DOM is
a continuous process.
The supply of DOM to a stream community is difficult to quantify. Fisher and
Likens (19 73), working in an upland stream,
found that almost 50% of the energy passing
through their study area was in the form of
DOM, half of which came from upstream
and half from groundwater entering the
study area. McDowell (1985), working in
Fig. 3. 12P activity of the collector insects Hydrapsyche californica and Simulium arcticum in an artificial stream. Controls 1 and 2 show levels when radioactive leaves and the insects were placed in the
stream for 7 d. Experiments l-3 show elevated levels
when the experiments were repeated with the addition
of a shredder species, Pteronarcys calijbrnica (from Short
and Maslin 1977).
the same stream, concluded that the rapid
precipitation of DOM is mainly an abiotic
adsorption phenomenon. Hynes (198 3) drew
attention to the need to make more detailed
studies of DOM inputs to river systems from
groundwater. He pointed out that groundwater may have an extremely long residence
time in the water table before being discharged into a riverbed and that the largest
quantities
enter the river through
the
streambed, from below. He suggested that
in the process, large quantities of DOM may
be precipitated and made available to the
infauna.
Lower reaches of streams- Farther downstream, the amount of in situ primary production increases. Periphyton algae may be
used by grazing invertebrates, but macrophytes mostly complete their growth cycles,
decay, and enter detritus food webs. Macrophytes such as Ranunculus, Potamogeton,
Nuphar, Typha, and other fringing reeds and
rushes all liberate DOM when they become
senescent and also contribute particulate
detritus that moves downstream with the
current. Cummins (1975) showed that there
is a tendency for the mean size of particles
in suspension to decrease with distance
downstream with the result that communities upstream tend to have a higher pro-
914
Mann
.IC _
T
= .oa
T
r.06
LARGE
LARGE
PARTICLES,
so.5 mm
ISOPODS, - II mm
- p\I
NUP
0
2 70$
8
65 ;; 60
25
2
do o”
,000
k
z
E"
-.04
8 .02
fr
0
PARTICLE
SIZE
(pm)
Fig. 4. Mean content of refractory organic matter
as a function of particle size in detritus collected from
eight running-water habitats (from Bowen 1984).
portion of shredders and browsers, while
the downstream communities have a higher
proportion of species that collect fine particulate matter. Bowen (1984) demonstrated that very fine particles often have no visible microscopic
structure, i.e. they are
amorphous and contain less refractory material (Fig. 4), so they are probably derived
from DOM by precipitation. Bowen (1984)
also showed that these particles are a good
source of nutrition to animals (Table 1); thus,
it is not surprising that the lower reaches of
rivers tend to support rich faunas of filter
feeders such as bivalve
molluscs
and
simuliid and chironomid larvae, as well as
deposit feeders in the sediments.
In running water, inputs of allochthonous
materials in the upper reaches and growth
of rooted macrophytes in the lower reaches
lead to a situation in which most river communities process the greater part of their
energy and materials through detritus food
webs rather than grazer pathways. Isotope
labeling of both particulate and dissolved
detritus fractions has demonstrated that detrital carbon and phosphorus does indeed
find its way into the invertebrates and, by
implication, into the fish.
An understanding of detritus pathways is
necessary for good river management. For
example, Bilby and Likens (1980) found that
natural organic dams in streams perform a
major role in processing organic detritus.
Pools form on the upstream side of the dams.
Sandy silt and fine organic particles accu-
SMALL
SMALL
PARTICLES,
co.5
ISOPODS,-4mm
mm
17
OF CONDITIONING
45
.I2
CI
G .I0
T
m.08
E
F .06
V
CK .04
tz
.02
0
0
7
DAYS
Fig. 5. Relative growth rates (RGR) of the isopod
Asellusforbesi when fed large-particle (above) and smallparticle (below) macrophyte detritus conditioned for
various lengths of time. Key to macrophytes: NUPNuphar h&urn; PEL- Peltandra virginica; SAU Saurus cernuus; PON-Pontederia
cordata. (From
Smock and Hawlowe 1983.)
mulate in the pools, retaining coarse organic
particles during the aging process of detritus. When organic debris dams were removed experimentally
from an upland
stream, the coarse organic matter was exported directly downstream in the unprocessed state, and the normal functioning of
the stream ecosystem was disrupted.
Detritus in lakes and marshes
The relative amounts of production by
macrophytes and by phytoplankton in lakes
vaq greatly according to the shape and
successional stage of the lake basin. There
are lakes with steep-sided rocky basins that
915
Detritus: Production and use
1
8
Consumption
0
m
I T
NO ANilBlOTlCS
ANTIBIOTICS
.I0
Growth
th
I
T Protein content
of food
,^ .08
I,
-I
tii
r.06
E”
-
.04
h
.02
Pet Sau
Pon
” Nup Pel Sau ‘Pon
MACROPHYTE
SPECIES
Pel
Sau
Pon
Fig. 6. Effect of aging macrophyte detritus with antibiotics. Figures show changes in food consumption and
growth of Asellus forbesi when feeding on the detritus and changes in protein content of food. Relative consumption rate--CR;
relative growth rate-RGR.
Key to macrophytes as in Fig. 5. (From Smock and Harlowc
1983.)
have minimal areas of littoral habitat and
associated macrophytes. At the other end
of the scale, there are shallow, eutrophi?
lakes in which the littoral zone extends almost to the middle of the lake. Such lakes
grade insensibly into marshes and wetland
where macrophyte production clearly dominates and almost all production of invertebrates and fish is supported by detritus
food webs. There have been numerous studies on the decomposition of wetland plants
such as Typha (Davis and van der Valk
1983), Nymphoides (Brock 1984), or Eichornia (DeBusk and Dierberg 1984) and
several useful reviews in Good et al. (1978).
As mentioned earlier, decomposition
of
macrophytes commonly found in the littoral zone of lakes follows the classical pattern: first, liberation of large quantities of
DOM; second, progressive shredding to
smaller particle size with increasing nitrogen content.
Smock and Harlowe (1983) studied the
food consumption and growth of the isopod
Asellus forbesi given detritus of various ages
derived from Nuphar, Peltandra, Saururus,
and Pontederia (Figs. 5, 6). They found that
the isopods grew better on ZVupharand Pel-
tundra, which had a higher protein content
than the other species. When the detritus
was aged for various lengths of time, there
was the expected initial increase in nitrogen
content, and this was reflected in improved
growth of the isopods. When aging took place
in the presence of antibiotics, the protein
content of the food and the growth of the
animals was correspondingly
depressed.
Clearly, Asellus benefits greatly by the accumulation of microbial protein during the
aging of macrophyte detritus.
Bowen (1979a, 198 1) reported from Lake
Valencia in Venezuela that the littoral zone
was occupied by dense beds of Potamogeton, the leaves of which were covered to a
depth of about 5 mm with a complex mixture of filamentous blue-greens, amorphous
organic detritus, diatoms, and sponges. This
material was the prime food of an introduced cichlid fish Sarotherodon (= Tilapia)
mossambicus which dominated fish biomass. The fish assimilate the total amino
acids of the aggregate with an efficiency of
63% (Fig. 7). Most of these dietary amino
acids were nonprotein in nature and were
believed to have originated from the precipitation of DOM. This is a clear example
Mann
SAROTHERODON
\
(=TILAPIA
I MOSSAMBICUS
PROTEIN
b
I
l/4
STOMACH
a
l
I
I
2/4
DIGESTIVE
I
3/4
TRACT
4/4
Fig. 8. Total organic content, protein content, and
algal volume of detrital aggregate samples taken from
sites of differing bottom slope in Lake Valencia, Venezuela (from Bowen 1979a).
SEGMENT
Fig. 7. Analysis of samples from stomach (on left)
and four successive quarters of the digestive tract of
Saroherodon mossambicus to show changes in protein
and total amino acids. Note large quantities of nonprotein amino acids (from Bowen 1980).
of fish production being supported directly
by detritus food chains.
A detailed study of periphytal detrital aggregate (PDA) in different parts of Lake Valencia (Bowen 1979a) showed that the slope
of the littoral bottom had a marked effect
on the composition of PDA (Fig. 8). On
steeply sloping sites, the aggregate was relatively rich in algae, protein, and total organic matter; on gently sloping sites, the
content of these materials was much lower.
Apparently, there is an accumulation on the
sand surface of old, refractory detritus
of low organic content. On gently sloping
shores, wave action suspends this material,
and much of it gets incorporated in the periphyton
aggregate. On steeply sloping
shores, the effect of wave action is to move
the refractory material offshore into deeper
water. As mentioned earlier, it was found
that nonprotein
amino acids were three
times as abundant as protein amino acids
in this detrital aggregate, and the fish were
able to extract the former as it passed slowly
through the gut. Whether these amino acids
occur singly or as polypeptides is not known.
A parallel study in Lake Sibaya, South
Africa (Bowen 19793, 1980, 1981), showed
a rather different set of feeding relationships. Sarotherodon mossambicus was pres-
ent and fed exclusively on detrital aggregate
that occurred as loose flocculated material
overlying a sandy bottom. The juveniles fed
on nearshore sand terraces, while the adults
fed in deeper offshore waters. The caloric
content of the detritus was about the same
in all areas, but the protein content varied
with depth from > 10% at depths of 0.5 m
o only 2% at 5 m (Fig. 9). Not surprisingly,
4 he juvenile fish grew rapidly and were
healthy, but the adults, which fed in deeper
Walter, grew slowly and appeared to suffer
from severe malnutrition.
The reason for
the higher protein content of shallow-water
detritus is not entirely clear, but it seems
probable that it is newly formed detritus
with a rich coating of microorganisms and
the detritus in deeper water is old and consists primarily of refractory material. When
th’e detrital aggregates of Lake Sibaya were
analyzed for amino acids, the content averaged 4.4% of organic matter, compared
with 14.6% in Lake Valencia. This difference probably accounts for good growth of
Sarotherodon in Lake Valencia, but poor
growth of the adults in Lake Sibaya. However, the ability of the tilapia family (Cichlidae) to make extensive direct use of detritus is good evidence of the transfer of
detrital energy and materials into species of
commercial interest.
In general, what proportion of lake primary production reaches fish by the grazing
pathway and what proportion by the detritus food web? It used to be assumed that
Detritus: Production and use
X
14
12
0
f
a 10
:
8
a-”
I
X
X
XX
I
26
z
ii
L’
E
2t
xx
x
x x
x
XX X
)$(xX x
xxx &
“%x
x
X
X
Fig. 9. Protein content of detrital aggregate samples
taken from various depths in Lake Sibava, South Africa
(from Bowen 19793).-
organic matter produced by phytoplankton
passed directly to grazing zooplankton and
thence to fish. In a major review of the
trophic relationships
of zooplankton
of
lakes and reservoirs, Hillbricht-Tlkowska
(1977) concluded that in most situations,
and especially in eutrophic lakes, more energy and materials reach zooplankton by detritus pathways than by direct grazing on
the living cells (Fig. 10). In eutrophic lakes,
the average biomass ingested by zooplankton is 5-l 5% small algae, lo-20% detritus,
and 70-85% bacteria; in oligotrophic lakes,
the proportion of small algae in the food
was up to 50%, with the balance made up
of detritus and bacteria. Larger algae, or
those forming colonial groups, appear not
to be readily consumed by freshwater zooplankton, but instead contribute particulate
and dissolved organic matter to detritus food
webs. When we also take into account particulate organic matter derived from macrophytes within the lake and allochthonous
material entering the lake from inflowing
streams or from the land, the possibilities
for zooplankton to derive much or even most
of their nutrition from detrital sources become very clear.
Detritus in estuarine and
coastal systems
Macrophyte detritus-Studies
of the fate
of marine macrophyte detritus were stimulated by Teal’s (1962) observation that, on
a salt marsh in Georgia, herbivores assimilated only 4.6% of the Spartina production,
leaving the remainder to enter detritus food
webs. Valiela et al. (1984) reported recent
work on a New England marsh and reviewed what is known about the decomposition of salt marsh grasses. Three phases
Mann
918
I
0
20
50
100
150
I
200
DAYS OF AGING
Fig. 11. Rcsulls of culturing the worm Capitella on
detritus prepared from three different sources and aged
for different times. Above-ratio
of worm production
to total oxidation in the cultures; below-ratio
of microbial biomass to total oxidation (from Tenore and
Hanson 1980).
were recognized: first, the leaching phase,
lasting < 1 month, during which 5-40% of
the biomass is lost; second, a decomposer
phase, lasting up to a year, during which
microbial
degradation
and subsequent
leaching of hydrolyzed substances removes
an additional 40-70% of the biomass; finally, the small fraction of refractory material remaining is slowly broken down over
an additional year. They showed that the
activity of invertebrates produces a small,
but significant increase in the decay rate,
while nutrient enrichment accelerates decomposition
up to 24%. Nutrient enrichment also has a qualitative effect on decomposition. When one or another nutrient is
limiting, the microbes on detritus tend to
release organic matter for processing elsewhere. When there is no limitation, microbial populations use the organic matter to
build up their populations on the litter (Howarth and Fisher 1976). The fate of other
vascular marine plants such as seagrasses or
mangroves is qualitatively
similar; however, rates of microbial decomposition are
variable and seem to depend not only on
the content of fibrous, refractory material
but also on various chemical defenses against
microorganisms or grazers. Thus, Harrison
and Chan (1980) showed that Zostera leaves
that had been dead up to 2 weeks contained
a water-soluble substance that inhibited the
growth of bacteria and algae. Also, Valiela
et al. (1979) showed that newly dead Spartina contains considerable amounts of ferulic and coumaric acids that are distasteful
to amphipods and snails and might be expected to slow the process of shredding and
grinding, which otherwise serves to accelerate the colonization of microbes.
13~ comparison with most vascular marine plants, algae have a much lower content
of fibrous material and a higher content of
nitrogen. When exposed to seawater under
field or laboratory conditions, algae decompose much more rapidly than marsh grass,
seagrass, or mangrove tissue. When a detritivore is included in laboratory experiments, the higher nutritive value and digestibility of the algae is reflected in a more
rapid and efficient assimilation of the detritus by the detritivore. These differences
are well illustrated by the experiments of
Tenore and Hanson (1980), who prepared
detritus from three sources: marsh grass
(Spartina), seaweed (Gracilaria), and natural mixed periphyton. Some detritus was
frozen soon after preparation; other subsamples were aged for different lengths of
tirne and then frozen. This made it possible
to run a series of parallel experiments under
standard conditions in which the polychaete
worm Capitclla was fed detritus from different plants aged for differing lengths of
time (Fig. 11). Worm production
was
measured, as well as microcosm oxidation
(the CO2 of the worm respiration plus the
amount of detrital carbon converted to CO2
in the process of microbial metabolism).
N’ote that the question being asked is very
close to the theme of this paper, i.e. in a
detritus-based system, what proportion of
the carbon enters invertebrate food webs
and what proportion is simply oxidized by
the microbes? The upper plot of Fig. 11
shows that the ratio of worm production to
microbial oxidation exceeded 80% for periphyton aged only 30 d. The seaweed Gracilaria needed aging at least 40 d and the
Spartina 200 d before a similar ratio was
re:ached. If seagrass tissue had been tested,
it would have required even longer (Har-
Detritus: Production and use
rison and Mann 197 5b). When the ratio of
worm production to microcosm oxidation
was high, it is probable that a high proportion of energy and materials from the detritus was going to invertebrates and a low
proportion to microbes. The lower part of
Fig. 11 shows microbial biomass as a function of microcosm oxidation and time of
aging and strongly suggests that it is the rapid buildup of microbial biomass on algal
tissue that makes possible the efficient utilization of this material by Capitella. However, the experiments of Findlay and Tenore (1982), mentioned earlier, also showed
that the worms derived much of their nitrogen through digestion of algal tissues.
Work with stable carbon isotope ratiosThe experiments with Capitella raise important questions. If vascular marine plants
are used relatively inefficiently by invertebrates over a 200-d period, and if meanwhile the fungi and bacteria convert much
of the detritus to CO*, how much of the
original plant energy and materials finally
reaches the invertebrates in a marine system
where vascular plant detritus is abundant?
Fortunately, stable carbon isotopes can be
used as tracers of vascular plant carbon in
marine food webs, and a partial answer to
our question has been obtained.
When the ratio of 13C to 12C in various
plants is measured and expressed as the conventional ?j13Cratio, Spartina tends to have
a value around - 12 to - 14a/oo,while benthic diatoms are around - 16 to - 18o/ooand
phytoplankton
is -20 to -22a/oo or even
more negative. The 613C value of detritus is
close to that of the material from which it
is derived, and that of animals is close to
the 613C value of their food, but with a tendency to be shifted 1-2Ym less negative (Fry
and Sherr 1984). Examination
of the 613C
ratios of animals in salt marshes or seagrass
beds therefore gives an indication of the extent to which the macrophyte carbon is getting into the animals through detritus pathways. The results suggest that, even in the
vicinity of dense macrophyte beds, periphyton, and benthic and planktonic algae make
a greater contribution than do macrophytes
to the carbon incorporated in invertebrate
tissues. For example, Haines (1976) and
Haines and Montague (1979) found that the
919
salt-marsh insects and snails had 613C values that corresponded with that of the Spartina; all other invertebrates, either intertidally in the marsh or subtidally in the creeks,
had 613C values that were more negative,
indicating a contribution
from benthic or
planktonic algae (Fig. 12). Using some simple assumptions, Hughes and Sherr (1983)
calculated that the contribution of Spartina
carbon to the carbon in animal tissues ranged
from < 10% in various fish like menhaden,
tongucfish, and pinfish to >40% in mummichog, with various invertebrates
like
crabs, shrimps, polychaetes, and squid occupying the middle of that range.
Unfortunately,
when there are more than
two sources of food, conclusions drawn from
the use of a single isotope such as 13C are
ambiguous. For example, in Fig. 12 there
are four food sources having 613C ratios
ranging from about - 12 to -26%0. An organism with a value of, say, -2 1 could arrive at that value by consuming mostly phytoplankton, or by consuming Spartina and
Juncus detritus in almost equal parts, or by
numerous other combinations of foods. This
kind of ambiguity can be resolved by the
simultaneous use of several isotopic markers. Peterson et al. (1985) studied the distribution
of 13C 15N, and 34S in upland
plants, Spartina, and plankton and in ribbed
mussels, Geukensia demissa. They were able
to show unambiguously
that the mussels
consumed Spartina detritus and plankton,
but not upland plant detritus. The mussels
nearer the center of the marsh consumed
mostly Spartina detritus, while those near
the edge consumed mostly plankton. This
suggests that organisms in coastal waters
outside the marsh were probably receiving
little Spartina detritus. Peterson et al. (1980)
proposed that bacteria using sulfide derived
from Spartina might fix carbon from seawater and thus have a 634Sclose to Spartina,
but a FL3C close to plankton. No evidence
that such sulfide oxidizers are an important
food source for marine invertebrates has so
far been brought forward.
Hopkinson and Hoffman (1984) made organic carbon budgets for the marsh-estuarine water and nearshore waters 6-l 0 km
from the coast of Georgia. They balanced
community
production,
respiration,
and
Mann
920
JUNCUS
SOURCE
MATERIAL
-
BENTHIC
DIATOMS
PHYTOPLANKTON
POM
SPARTINA
CREEKS
-
SALT MARSH INSECTS
SALT MARSH SNAILS
DEPOSIT-FEEDING
CRABS
n MUD
SNAILS
RIBBIED MUSSELS
-
INTERTIDAL
INVERTEBRATES
n
m OYSTERS
MUD CRABS
SQUIID
I SHRIMPS (PALAEMONETES
n BLUE
CRABS
BROWN SHRIMPS
n
n
SUBTIDAL
INVERTEBRATES
(DUPLIN
RIVER)
n
PENAEUS)
- OYSTERS
n
FISH
(DUPL IN RIVER)
n
= MENHADEN
II1
-25
-20
MUMMICHOG
(FUNDULUS)
MULLET (MUGIL)
(B’REVOORTIA)
I
.I
-15
613C
-10
Fig. 12. Stable carbon isotope ratios of detritus source materials, intertidal
fish in a salt-marsh area in Georgia (from Haines 1976; Haines and Montague
storage against known imports and exports
from the two systems. They found that production exceeded respiration in the marshestuary, providing for a net export to the
turbid inner coastal zone. In this zone, respiration exceeded primary production by
210 g C me2 yr-I, which Hopkinson and
Hoffman believed to be supplied by organic
inputs by rivers and by export from the
marsh-estuary region. Knowing the input of
the rivers, they concluded that about 5% of
net marsh production is required to balance
the carbon budget of the turbid inner coastal
waters. At this low level of dependence of
the coastal waters on the salt-marsh production, it is not surprising to find that
Spartina carbon constitutes a minor proportion of the carbon of subtidal invertebrates and fish.
Analogous studies have been made in and
around seagrass beds in various parts of the
world. Thayer et al. (1978), working in the
southeastern U.S.A., concluded that seagrass carbon makes a significant, but not
dominant contribution
to the food web of
a Zostera bed. McConnaughey and McRoy
-5
0
RATIO
and subtidal invertebrates,
1979).
and
(1979) concluded that some invertebrates,
such as sea stars and clams living in a seagrass bed in Alaska, derived about a quarter
of their carbon from the seagrass and the
remainder probably from periphyton and
Shrimps and polychaete
phytoplankton.
worms derived even less from Zostera.
Hence, in temperate and cold waters, the
processing of seagrass tissue through detritus food webs appears to play a minor part
in supporting invertebrates and vertebrates.
In the tropics, plankton productivity tends
to be limited by the existence of a permanent thermocline and low nutrient levels in
surface waters, and the contribution
of seagrass beds may be more significant. Fry and
his coworkers (Fry and Parker 1979; Fry et
al. 1982, 1983) compared the 613C ratios of
animals taken offshore with those of the
same or similar species taken from seagrass
beds. Those from the seagrass beds were up
to 8.3o/ooless negative than those from offshore, indicating that there was a substantial
contribution
of macrophyte carbon. These
results were obtained in the Torres Strait,
in the Caribbean, and off the coast of Texas.
Detritus: Production and use
Similarly, Rodelli et al. (1984) found that
the 613C ratios of the leaves of mangroves
were much more negative than those of phytoplankton
or benthic algae. Of the 5 1
species of animals they studied, 29 had ratios more negative than the algae, indicating
a component of mangrove detritus in the
diet, and this included some commercially
important species of bivalves and shrimp.
Summarizing
this section, detritus derived from vascular marine plants tends to
have a high fiber content and low nitrogen
content, so that it requires an extensive period of conditioning by microorganisms before it constitutes nutritious food for animals. In environments where less refractory
algal detritus is readily available, animals
may always grow up with more algal carbon
than vascular macrophyte carbon in their
tissues.
The utilization
of seaweed detritus-As
one might expect, the 613C values of macroalgae are close to those of phytoplankton
algae, so stable carbon isotopes are not good
tracers in studies attempting to discover the
relative importance of seaweeds and phytoplankton in the diet of coastal invertebrates and fish. For example, Stephenson et
al. (1984) showed that the blades of Laminaria longicruris had 613C values ranging
from - 12 to -20%0, according to the part
of the blade from which the sample was
taken, although phytoplankton
(or more
precisely, POC filtered from seawater) from
temperate shelf and open estuarine waters
normally lies between - 18 and -24?& (Fry
and Sherr 1984). In a subsequent paper (Stephenson et al. 1986), the 613C ratios of animals taken from a kelp bed were compared
with the ratios in animals of the same species
taken from a seagrass bed. Only the small
grazing gastropod Lacuna vincta had significantly different ratios, indicating that it
was using carbon from the plants on which
it crawled, while Littorina littorea from the
eelgrass bed had the same ratio as the snails
from the kelp bed, suggesting that both may
have been taking mainly periphyton. Bedford and Moore (1985) made an intensive
study of feeding and growth of the polychaete Platynereis dumerilii, which lives
primarily on sublittoral accumulations
of
drifting kelp, Laminaria saccharina. The
921
worms were found to ingest fresh detritus
in preference to fronds in an advanced stage
of decomposition.
They grew well on this
diet and appeared to be a clear example of
detritivores that derive their nutrition directly from the plant material without much
assistance from microorganisms.
Kelps of the group Laminariales have a
very diverse morphology but most, if not
all of them, have an active growth zone at
the base of the blade and a zone of erosion
at the tip of the blade. They tend to release
particulate and dissolved organic matter
from the erosion zone at all times of year,
thus providing a continuous and dependable source of detritus for the invertebrates
in the area. Perhaps the best documented
study of a detritus food web in a kelp community is that carried out on the west coast
of Cape Peninsula, South Africa, under the
leadership of J. Field (Field et al. 1977;
Newell and Field 1983; Wulff and Field
1983) and recently reviewed by Newell
(1984) (Fig. 13). The kelp beds, dominated
by Ecklonia maxima and Laminaria palZida, produced about 500 g C m-2 yr- 1 of
POM and 250 g C me2 yr-1 of DOM. Phytoplankton production in the area was also
about 500 g C m-2 yr-1 . If the system were
closed, the combined phytoplankton
and
kelp production would just about supply the
nutritional needs of the filter-feeding invertebrates. The mussels had enzyme systems
capable of digesting the carbohydrates contained in the kelps (Siederer et al. 1982;
Stuart 1982). By an ingenious double-labeling technique, Stuart et al. (1982) showed
that the mussels in the kelp bed wcrc deriving much of their tissue carbon from the
plant material rather than relying on the
colonizing bacteria.
The Cape Town kelp beds are adjacent to
the Benguela upwelling system. During upwelling the filter feeders receive predomininantly kelp detritus, and at the time of
downwelling
they receive mostly phytoplankton carbon. A simulation model (Wulff
and Field 1983) showed that the relative
importance of phytoplankton
and detritus
to the filter feeders depends on the frequency of upwelling and on the rate of water
movement through the kelp beds. With realistic figures for these variables, it was
922
Mann
PRIMARY
PRODUCTION
FRAGMENTATION
BACTERIAL
DECOMPOSITION
Bacteria
4084
CONSUMPTION
)
C = 67541
Filte*,,,i;,
herbivores
P = 5625
y
Fig. 13. Simplified energy flow diagram for a kelp bed on the west coast of Cape Peninsula,
Numbers in boxes represent fluxes out of those boxes, in kJ m-2 yr-I (after Newell 1984).
shown that the kelp made an important contribution.
The invertebrate
filter feeders
supported a valuable stock of rock lobsters,
so this is a good example of detritus pathways supporting a commercially important
species. Observations in North America and
Australia (reviewed by Mann 1982) show
that kelp beds around the world provide
habitat and trophic support for valuable
lobster stocks.
A separate study of the fate of kelp biomass cast up on beaches near Cape Town
(Koop et al. 1982a,b) showed that invertebrates consumed 74% of the kelp within
8 d and bacteria consumed the remaining
26%. Invertebrate feces amounted to 67%
of the kelp carbon and were in turn, metabolized by bacteria in the sand. Overall,
100 g of kelp carbon yielded 23-28 g of
bacterial carbon available to higher trophic
levels, but the startling finding was that this
bacterial biomass contained 94% of the nitrogen originally present in the kelp. Very
few studies of detritus food webs have produced budgets of both carbon and nitrogen.
When we conclude that, in some situations,
z4
South Africa.
a relatively small proportion of detrital carbon enters invertebrate food webs, we should
perhaps ask whether the proportion of nitrogen entering such webs is markedly different.
Detritus in planktonic marine systemsThLeidea that detritus-based food webs might
be important in planktonic marine systems
was given early impetus by the work of Baylor and Sutcliffe (1963) and Sutcliffe et al.
(1963) on the physical transformation
of
DOM to POM in the sea. Since the mass of
DOM in the oceans is much greater than
the biomass of living organisms, the potential biological significance of converting
DOM to particles that animals could eat
appeared to be considerable. The role of
POM in the sea was critically reviewed by
Riley (1970), who described various types
of aggregates and their relationships with
microbes. Then Pomeroy (1974) wrote a
challenging paper entitled “The ocean’s food
we:b: A changing paradigm.” He drew attention to the fact that very small cells, nannoplankton and picoplankton, are probably
more important as primary producers than
923
Detritus: Production and use
the well-known diatoms, and that these may
be consumed by microzooplankton,
about
which we have very little information. More
importantly from the point of view of this
paper, he drew attention to the large fraction
of community
respiration attributable
to
bacteria-sized microorganisms, and he postulated that the fuel for this metabolic energy was detritus, derived from animal feces
and from the DOM excreted by phytoplankton. Pomeroy (1979) followed up his ideas
with a modeling exercise in which he showed
that it was entirely feasible for more than
half of the products of photosynthesis to
pass through detritus pathways, without the
observed relationship
between total primary production and total fish production
being violated. Pomeroy (1980) provided
descriptive material to flesh out his ideas
on planktonic marine detritus food webs,
showing the flocculent and flake-type aggregates of POM that are probably derived
from DOM by physical precipitation,
the
bacteria that feed on them and in turn produce strands of extracellular material, and
examples of morphous detritus found within copepod fecal pellets.
The question of how important detritus
food webs are in supporting invertebrate and
fish production in marine food webs is not
yet settled. It is easy to show, using widely
accepted conservative
assumptions,
that
more phytoplankton carbon is processed by
detritus pathways than by grazing pathways.
As an example, in Fig. 14 (from Newell
1984) we start with 100 g C of phytoplankton production. If the herbivores consume
80 g C, 10 g C is left to decompose and 10
to sink below the thermocline. If the herbivore assimilation efficiency is 50%, then
there is 40 g C of fecal pellet production.
Already 10 + 10 + 40 = 60 g C has entered
detritus pathways, compared with 40 assimilated by the herbivores. Such a budget
leaves unanswered the question of what
proportion of the detrital energy and materials ends up in stocks of commercial interest. Goldman (1984) discussed the problem of how phytoplankton
cells can
maintain high rates of division in a lownutrient medium such as the oligotrophic
ocean. Developing the ideas of numerous
earlier workers, he put forward the “aggre-
=e
Thermocline
m
Primary productlon
Settlement
from
photic zone
Fig. 14. Diagram to show how the greater part of
the energy
-_ in a marine planktonic system would inevitably pass through detritus pathways. Herbivore consumption- C; respiration-R;
growth production - P;
feces production-F.
“Oxidized carbon” refers to carbon that has passed through detritus pathways. From
an initial 100 g C, 49.4 in the photic zone plus 9.6
below the photic zone (i.e. 59 g C)pass through-detritus
pathways (from Newell 1984).
gate spinning-wheel concept” in which nutrient cycles proceed rapidly in discrete
communities attached to detritus particles
(Fig. 15). The community consists of small
phytoplankton,
bacteria which utilize the
DOM produced by the phytoplankton
(up
to 50% of gross photosynthesis in nutrientlimited
situations),
and microflagellates,
which consume both autotrophs and bacteria. He then suggested that in the “contemporary food chain concept,” these aggregates are the most important food source
for grazers. The parallel between these ideas
and those of Bowen (1984) on amorphous
detrital aggregates in freshwater is very
striking. Azam and Ammerman
(1984),
speculating along the same lines as Goldman, invoked a “cluster hypothesis”
in
which bacteria cluster around phytoplankton cells, making optimal use of the excreted DOM and regenerating nutrients.
Mann
924
PAR
\/
,?;. . .
..‘. .
..:.
..:.. . . .
’
.
.f-)o&.
/
y
measure the latter. For example, Hargrave
(1973, 1975) used this technique to determine that the sedimentation of organic carbon, S, is proportional to primary production, C, (as measured by 14C uptake), and
inversely proportional
to the mixed layer
depth, Z,,, according to the equation
s = 4.9 + 3.9g
Fig. 15. Diagram of a postulated “aggregate spinning-wheel”
community
of phytoplankton,
bacteria,
and flagellates on an amorphous detrital aggregate (from
Goldman 1984).
Williams (1984) discussed whether the
very considerable biomass of bacteria in the
sea is contributing significantly to food web
productivity
or whether it is mainly mineralizing the materials on which the bacteria
feed. He concluded that there is insufficient
evidence to provide an answer. Azam et al.
(1983) postulated that the bacteria are indeed extensively grazed by heterotrophic
flagellates and microzooplankton,
which in
turn are preyed upon by larger zooplankton.
They pointed out that this is a mechanism
for returning DOM released by phytoplankton back to the main food chain and called
the mechanism a “microbial
loop.” The
evidence for such a pathway had already
been reviewed by Mann (1982), but convincing evidence from the natural environment is still lacking. For example, Tanoue
and Hara (1986) showed that Antarctic krill
feed heavily on choanoflagellates, which in
turn feed on bacteria, but the relative importance of this pathway compared with that
based on diatoms has not yet been demonstrated.
Detrital food webs in the marine benthos-If
we consider the oceans as whole,
by far the greater part of the sea floor is
below the photic zone; thus, its communities depend entirely on the rain of detritus
to provide energy and materials for food
web productivity.
One way of quantifying
the flux of detritus into such systems is to
ignore any net accumulation in sediments,
assume a balance between input of detritus
and metabolism of the community,
and
?,Z
whlen sedimentation and production are in
g C m-2 yr- l. The probable explanation is
that in a deep mixed layer, the phytoplankton is kept in suspension by turbulence long
enough for the zooplankton
to consume
most of it. When the mixed layer is shallow
(as in many coastal waters), however, a good
proportion of the phytoplankton
sinks rapidly through it to less turbulent waters below
the thermocline and then continues on to
the bottom. The net result is that in coastal
waters with primary production on the order of 200 g C mm2 yr-l, up to 80 g C m -2
yr-. l may reach the bottom, whereas in the
great ocean basins, < 5 g C m-2 yr- l reaches
the bottom.
One of the interesting questions about the
processing of detritus in benthic communities is this: If the carbon in the detritus
were to be processed through the food chain,
as follows:
organic detritus -+ bacteria --$
ciliates + meiobenthos -+
macrobenthos,
with an ecological efficiency of 10% at each
step, the net overall efficiency of macrobenthos production as a percentage of detrital
input would be only 0.0 1%. At 20% efficiency at each step it would be only 0.16%.
Yet, models of benthic fish production demand an efficiency of something like 20%
overall (Steele 1974; Mills 1975). Clearly,
the postulated food chain is quite wrong.
The evidence was reviewed in detail by
Mann (1982: chapter 7), and the most logical explanation
seems to be that many
prominent macrofaunal species such as the
filter-feeding
bivalves and polychaetes,
browsing epifauna such as gastropods and
amphipods, and even tube-dwelling infauna
are capable of intercepting newly settled de-
Detritus: Production and use
tritus at the sediment surface and using it
directly with an efficiency up to 40%. It is
worth noting that in many coastal waters,
bottom-feeding
fish constitute 30-50% of
the commercial catches, and these benthic
detritus food webs, so poorly understood,
are directly responsible for supporting these
valuable fisheries. Some indication of the
kinds of adaptations that may make possible this high efficiency of detritus use are
the demonstrations
by Foulds and Mann
(1978), Wainwright and Mann (1982), and
Friesen et al. (1986) that the epibenthic mysid, Mysis stenolepis, can digest cellulose
with endogenously produced enzymes, or
that of Fong and Mann (1980) that sea urchins have a gut flora that can digest cellulose.
In shallow water and intertidal areas, living benthic diatoms are available to supplement the detritus accumulating at the
sediment surface. Stuart et al. (1985) showed
that the amphipod Corophium volutator
feeds mainly on benthic diatoms during the
spring-summer period when its population
growth is most rapid, but that it relies on
Spartina detritus to carry it through the fallwinter period when diatom biomass is low.
There is indirect evidence from a number
of sources that although fresh algal cells are
a superior food source to detrital particles,
they are often available for only a part of
the year, and that detritus particles, which
tend to be available year round, serve as a
supplementary food source to carry the invertebrates through periods of low algal
abundance.
An ecosystem view of detritus
Up to now, this paper has had a rather
anthropocentric flavor, revolving around the
question of how important detritus is in
supporting food webs leading to fish or
shellfish. By implication, detrital carbon that
is converted to CO, in bacterial respiration
is “wasted.” Many contemporary ecosystem theorists have quite a different point of
view (for review, see Rich 1984a,b, 1988)
that can be traced back to Herbert Spencer
with important contributions
by Lovelock
and Prigogine. The essence is that life and
the physicochemical
environment
of the
biosphere coevolved in a mutually depen-
925
dent manner, beginning about 3.6 billion
years ago with the origin of self-reproducing
organisms in a virtually oxygen-free atmosphere. During the Proterozoic Eon (2.60.6 x log yr B.P.), photolithotrophy
evolved
into photosynthesis, electrons were transferred from the environment
to organic
matter, and organic matter was transferred
to the lithosphere by sedimentation. During
this period, the oxygen concentration of the
atmosphere rose from essentially zero to
about 20%; there resulted a redox potential
of about 1.5 V between upper aerobic environments and sedimented anaerobic environments. The scene was set for the evolution of eucaryotic cells and ultimately
invertebrates and vertebrates. In this view
of the world, the energy captured by photosynthesis is not stored in the products of
photosynthesis but rather between the products of photosynthesis as redox potential
(Rich 1988). Detritus in the modern world
is seen as the vestige of conditions that existed before the evolution of eucaryotes.
Respiration of eucaryotes is a process that
also evolved in the Proterozoic Eon, providing the energy for predation (both herbivorous and carnivorous) and hence for
food web linkages. Detailed consideration
of the “evolutionary
arms race,” in which
prey evolved defenses against predation by
increasing their content of indigestible material, leads to the view that detritus production from feces, etc., is an inevitable
concomitant
of predation, and that processes leading to fish and shellfish production (regarded by man as desirable) must of
necessity be accompanied by detrital processes that renew the pool of electron-rich
sedimented organic matter and, indirectly,
maintain the environment
for ecosystem
function.
When biosphere function is viewed in this
detached manner, man’s preoccupation with
maximizing the production of vertebrate and
invertebrate food is seen as a trivial concern
compared with the need to maintain a viable environment for the whole biosphere
process. If predatory food webs and detritus
are simply two essential aspects of heterotrophy, it is idle to speculate on whether
detritus food webs are important. It is analogous to the question, at the organismal
926
level, is respiration
than growth?
Mann
more or less important
Conclusions
The principles of detritus production and
utilization are the same in all aquatic habitats. Dead organic matter takes two forms,
dissolved (DOM) and particulate (POM),
and most of the earlier work was concerned
with the fate of POM. It is now known,
however, that DOM is readily converted to
POM by physical and biological mechanisms, so that the two forms must be considered together.
Many aquatic plants give off substantial
quantities of DOM both during life and soon
after death, and it is now believed that a
large proportion of this is quickly taken up
by bacteria and converted to living bacterial
biomass or to slimelike aggregates. Another
fraction is converted to particulate form by
physical precipitation,
particularly
at the
surfaces of bubbles or on rocks or plant surfaces. In streams, DOM originating from
allochthonous
or autochthonous
plants is
rapidly deposited on streambeds and colonized by bacteria, fungi, and algae, which
form a nutritious aggregate that is readily
used by stream invertebrates.
In lakes,
a,morphous detrital aggregates believed to
be derived from DOM are found in suspension, deposited on plant surfaces, and
lying on the sediments. They are readily used
by fish and amphibia.
It is in planktonic systems of lakes and
the sea that our knowledge of the fate of
DOM is most uncertain. Many now believe
that bacteria are closely associated with
phytoplankton and make optimal use of the
DOM released by them. It is further suggested that floating detrital aggregates support communities of organisms that include
protozoa, which continuously
feed on the
bacteria, and that the aggregate communities are themselves consumed by copepods
and other zooplankton.
The fate of the particulate detritus left
behind after the initial leaching of DOM
depends on whether the source is vascular
or nonvascular.
Much algal material is
readily digested and used by invertebrates
without further transformation.
Vascular
material, on the other hand, has a high con-
tent of cellulose, lignin, etc. (which most
animals cannot digest) and has a lower content of amino acid nitrogen. Extensive work
during the 1970s showed how such material
is colonized by bacteria, shredded by invertebrates, and progressively enriched in
nitrogen while the content of refractory material is being reduced. After a prolonged
period of such conditioning, vascular detritus becomes nutritious
for invertebrates.
However, there is a subsequent phase in
which much of the nitrogen in the detritus
becomes bound to large molecules such as
phenolics, which resist digestion by detritivores (Rice 1982; Melillo et al. 1984).
The question with which we began- How
important are detritus food webs in supporting the secondary productivity
of commercially important species?- can now be
partially answered. In the upper reaches of
rivers, detritus derived from terrestrial
sources is often the dominant source of energy and materials and undoubtedly
supports fish production. In the lower reaches
of rivers, production by benthic algae and
aquatic vascular plants becomes the major
source of nutrition, and detritus food webs
still1 predominate. In lakes, detritus pathways are undoubtedly important in littoral
zones; it has been claimed that even in the
plankton, more energy and materials are
transferred to zooplankton by detritus pathways than by direct grazing.
The earlier idea that the productivity
of
coastal marshes and seagrass beds supported coastal fisheries seems not to have been
confirmed by recent studies, although questions still remain. In any case, it is abundantly clear that seagrass beds provide an
important habitat for many species. On the
other hand, seaweed detritus appears to be
utilized very effectively in coastal food
chalins leading to shellfish production. The
question of whether the conventional phytoplankton-zooplankton-fish
food chain is
predominant
in open ocean waters or
involving
whether the “new paradigm”
DOM, bacteria, and protozoa is of paramount importance is an open question and
a challenge to contemporary
biological
oceanography.
Several points emerged from -this comparison of freshwater and marine systems.
Detritus: Production and use
One point is that the pathway of DOM from
the plant which generates it, through its
physicochemical
precipitation
as amorphous POM, to its utilization
by invertebrates, fish, and amphibia has been much
better documented in freshwater than in
marine environments (e.g. Bowen 1979a, b,
1980, 198 1, 1984). Estuarine ecologists have
much to learn from this work, and it will
be interesting to know whether the juvenile
fish that forage in such large numbers in
shallow estuarine waters are making as extensive use of precipitated DOM as Tilapia
(Sarotherodon) has been shown to do in
lakes. These fish obtain much of their nourishment by browsing on the periphyton zone
of rooted plants; an investigation of the epiphytic zone of seagrasses might reveal that
these also play a role as surfaces for the
precipitation of DOM that subsequently enters invertebrate and vertebrate food webs.
The firmly established link between detritus
food webs and the growth and productivity
of a commercially important freshwater fish
is the best evidence available for the “usefulness” of detritus from man’s point of
view. It seems probable that similar links
will eventually be established for the estuarine-marine environment.
It is also instructive to think about the
stratification
with depth of detritus food
webs in freshwater and marine environments. As Bowen (1979a) showed, there is
a natural sorting of detritus in the littoral
zone of lakes, especially on shores with a
steep slope. New amorphous POM is continually being formed in the shallow water
under the influence of wave action, and the
readily utilizable material becomes incorporated in higher trophic levels while refractory material tends to accumulate and
move down the slope to deeper water. The
result is that nearshore detritivores have a
nutritious diet, while organisms farther offshore do less well. It would be surprising if
similar processes were not at work in estuarine and coastal environments,
though
modified by the influence of tides. Camilleri
and Ribi (1986) showed how the process
may work in mangrove forests, and Velimirov (1986) studied DOC dynamics in a
Mediterranean seagrass system.
An analogous vertical zonation occurs in
927
sediments of both lakes and coastal waters.
Fresh, labile detritus accumulates at the
sediment-water
interface and is exploited
by a suite of invertebrates (e.g. chironomid
larvae: Jonasson and Kristiansen 1967; gastropods and bivalves: Rhoads 1974). A proportion of the organic matter becomes buried by bioturbation,
but this tends to be
more refractory material. The net result is
that vertical profiles show a high carbon
content at the sediment surface, with a progressive decrease with increasing depth. The
first few centimeters are aerobic, but below
a certain depth, depending on the grain size
of the sediments and the amount of surface
disturbance, the sediments are rendered anaerobic by the respiration of the microorganisms, and anaerobic bacteria become active. Relatively few invertebrates inhabit the
anaerobic layers, and it is thought that anaerobic fermentation at these depths results
in a supply of DOM which diffuses upward
and enters the pool in the overlying water
(Wiebe 1979).
Perhaps the strongest message from this
freshwater-marine comparison is that, while
research over the past lo-20 yr has paid
most attention to the processes associated
with fragmentation and decay of vascular
plant detritus, it now appears that the fate
of the DOM released in the early stages of
decomposition
may be ecologically more
significant. In planktonic environments, the
detailed relationship between the DOM released by phytoplankton,
the bacteria that
take it up, and the protozoa that consume
the bacteria (“microbial loop”) promises to
be a fertile line of enquiry.
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