Download Bacterial-Invertebrate Interactions in Uptake of Dissolved Organic

AMER. ZOOL., 22:723-733 (1982)
Bacterial-Invertebrate Interactions in
Uptake of Dissolved Organic Matter1
DIETRICH SIEBERS
Biologische Anslalt Helgoland (Zentrale), Notkestrafie 31, D-2000
Federal Republic of Germany
Hamburg-52,
SYNOPSIS. AS compared to integumentary uptake systems of soft-bodied marine invertebrates, bacterial systems, in terms of transport constants, are much better adapted to
the low concentrations of dissolved organic nutrients encountered in coastal and offshore
waters. Bacteria respond to the presence of suitable dissolved organic substrates with
induction, uptake and multiplication, maintaining the concentrations of dissolved organic
matter (DOM) permanently low. At realistic in situ concentrations, epidermal uptake by
pelagic and epibenthic animals proceeds at such low rates that scarcely a substantial proportion of their metabolic needs is provided by absorption. In marine sediments, where
the life processes of bacteria and animals are closely interrelated, the macrofauna is sheltered by shells, firm tubes and burrows, which are irrigated by means of overlying water
of the water column. Hence, interstitial water with its sometimes higher concentrations
of DOM is scarcely available to sediment-dwelling larger metazoans. The meiofauna mainly inhabits the few millimeters of the upper sediment layers and the thin halos surrounding
irrigated macrofaunal burrows, where sufficient oxygen is available. Unless the magnitude
of horizontal water movement, the amounts of diffusional nutrient supply and the percentages, by which nutrient concentrations are reduced by meiofaunal uptake, are known,
estimations of nutritional benefits from uptake of DOM by meiofauna cannot be made.
For all infaunal taxa, bacteria appear to represent a major food supply.
INTRODUCTION
9
The biomass of 2 x 10 1 C in the world
oceans is small, when compared to
919 x 109 t C of the living resources on
land. As outlined in Table 1, the comparison of 2 x 109 t organic carbon bound to
marine organisms with 200 x 109 t dissolved in the oceans (DOM) points to the
unexpected fact that only about 1% of organic matter in the sea is encountered in
living organisms. The net primary production of 28 x 109 t C yr"1 in the sea,
which amounts to about half of the primary production on land, is performed by
a marine biomass roughly 500 times smaller than terrestrial living material (Whittaker and Likens, 1975).
The organic matter dissolved in the
oceans varies with respect to total concentrations, composition, relative proportions
of individual components, geographic location, water depths, season and the presence and physiological state of microbes,
1
From the Symposium on The Role of Uptake of Organic Solutes in Nutrition of Marine Organisms presented
at the Annual Meeting of the American Society of
Zoologists, 27-30 December 1980, at Seattle, Washington.
plants and animals. Steady-state concentrations of DOM are the result of input
processes comprising losses in primary
production, detritus products of the food
chains, autolytic degradation in decaying
animal and plant materials and terrigenic
sources (Fig. 1). Processes reducing the
level of steady-state concentrations include
self aggregation, adsorption to inorganic
detritus surfaces finally leading into food
chains, and heterotrophic absorption by
marine bacteria, yeasts, fungi, algae, protozoa and metazoa. While the major proportion of DOM is refractory to organismic utilization, the smaller part, present at
low levels in all natural water bodies, plays
diverse biological roles as nutritive sources
for all kinds of heterotrophs, as agents for
communications and interactions, orientation and migration, as vitamins, marine
toxins, and in interrelations with trace elements which are chelated and thus controlled and kept accessible for autotrophic
utilization. Considering the various aspects
mentioned, we will concentrate in the following on the role of amino acids and other dissolved organic substances in the nutrition of bacteria and soft-bodied
invertebrates and interrelations and competitions possibly occurring thereby.
723
724
DIETRICH SIEBERS
T A B L E 1. Global distribution of biomass, occurrence of
organic carbon in the sea, and net primary production. *
Land
Biomass
919
Participate
organic C
Losses during
primary production
Sea
2
- 109 t C
20
• 109 t C
(
Detritus products^
of the food c h a i n /
(Autolytic processes)
Terrigenic material)
Dissolved
organic matter
(DOM)
200
• 109 t C
Steady-state concentration
Net primary
production
59
28
• 109 t Cy-1
of dissolved organic matter
* Modified from Whittaker and Likens, 1975.
I
For heterotrophic bacteria, absorption of
dissolved substances represents the sole
source of nutrition. Assumptions that animals also, besides ingestion and processing of paniculate food within alimentary
canals, can take up dissolved nutrients
across the skin at rates securing uptake of
a significant proportion of their nutrition,
have been met with skepsis and rejection
for decades. The discussion of the question as to whether marine invertebrates can
and do obtain a noteworthy amount of energy and matter from these uptake processes reaches back to the dispute between
Putter and Krogh in the twenties.
Summarizing the pertinent literature on
integumentary transport of dissolved organic molecules across soft body surfaces
of invertebrates, one comes to the conclusion that all species belonging to all major
taxonomic phyla investigated in this respect possess this capacity, which fulfills all
prerequisites to be termed "active transport," such as the enormous concentration
gradients between ambient medium and
cell interior, substrate specificity and the
utilization of biological energy. The dependence of integumentary amino acid and
monosaccharide transport on ambient salinity and sodium confines these processes
to inhabitants of estuarine and marine
waters. In fresh water active solute uptake
by protozoa and metazoa apparently does
not occur, and cycling of organic nutrients
is exclusively performed by bacteria.
The question which arises on the subject
( Self - aggregation )
I
Adsorption to
( inorganic detritus particles
^ e n t r a n c e to food chainsy
(
Heterotrophic absorption \
(bacteria, yeasts, fungi, 1
algae, protozoa, metazoa) 7
FIG. 1. Processes leading to steady-state concentrations of dissolved organic matter.
of feeding on dissolved organic substances
in marine biota is, however, less concerned
with the mere presence of uptake properties within animal integuments, than with
quantitative aspects including nutrient
concentrations and availabilities, kinetics
data of the uptake systems and the relation
between heterotrophic biomass and dissolved food. It has to be investigated,
whether, under the given conditions of
marine habitats, dissolved organic molecules actually play a major role in the nutrition of the soft-bodied invertebrate fauna—as suggested by several authors,
including speakers of this symposium—and
whether uptake by animals proceeding in
competition with bacteria significantly contributes to the processes which reduce
steady-state levels of DOM. The habitats
which must be considered separately on
ecological and structural grounds are the
water column and the sediments. It is not
the aim of this report to present an extensive review of the literature available; on
BACTERIAL-INVERTEBRATE INTERACTIONS
the contrary, the problem mentioned will
be discussed within the framework of a few
selected relevant communications.
PRIMARY DECOMPOSITION OF DETRITUS
725
food by means of alimentary canals. No
publications are available demonstrating
the successful maintenance of any free-living aquatic protozoa or metazoa exclusively on dissolved food.
The dominating primary decomposers
HETEROTROPHIC ABSORPTION IN
of dissolved and paniculate detritus in ecoTHE WATER COLUMN
systems are bacterial populations (Fenchel
and J0rgensen, 1977). In this context the
The abovementioned concepts will be ilterm detritus means all non-living organic lustrated by means of two examples, one
material, including dissolved substances, of which is concerned with the fate of glulost by non-predatory pathways from any cose in an estuary, the other with amino
trophic level and, additionally, materials acid uptake in a sea star.
delivered from sources external to the ecoThe source and fate of glucose in the
system (allochthonous organic carbon) Duplin River (Sapelo Island, Georgia)
(Wetzel et at., 1972; Fenchel and J0rgen- Spartina alterniflora salt marsh estuary was
sen, 1977). As compiled by Sepers (1977) investigated by Hanson and Snyder (1980).
bacteria are especially adapted to the low Significantly higher concentrations of gluconcentrations of dissolved organic matter cose in afternoon samples than in those
encountered in most natural habitats in collected in the morning and the finding
possessing higher affinity uptake systems that a relatively high glucose concentration
with transport constants 100- to 1,000-fold correlated with a high concentration of
below those of animals. Bacteria can ab- chlorophyll a suggest primary production
sorb inorganic micronutrients such as ni- as the main source of this monosaccharide,
trate and phosphate and simultaneously which is the dominant low molecular sugar
hydrolize micronutrient-poor plant mate- in all natural dissolved carbohydrate mixrial as well as animal tissues by means of tures. Within the marsh system, Spartina
extracellular enzymes. The liberated alterniflora, phytoplankton, and benthic
monomers are absorbed from solution. algae were the most obvious sources of gluBacteria possess effective metabolic switch cose. The major glucose utilizers in the rivon/switch off mechanisms to survive long er system were probably microheteroperiods of low or negligible food supply trophs, bacteria, yeasts and possibly some
and to react rapidly to available suitable algae using extremely low glucose concennutrients.
trations, which were generally below 20 /u.g
1
The well-documented superiority of liter" at 1relatively fast rates of 2—5 fig libacterial uptake systems, especially with ter~' hr" . These concentrations of about
respect to substrate affinity, is the strong- 0.1 (iM glucose are roughly ten times lowest argument for the assumption that bac- er than lowest levels tested in uptake exteria permanently keep the concentrations periments with soft-bodied invertebrates.
of all dissolved nutrients at the low levels Consequently the authors argue that at
encountered in natural biota, which do not, these low monosaccharide concentrations
as a rule, allow pelagic and epibenthic soft- and with respect to the high microheterobodied invertebrates to compete success- trophic uptake rates mentioned it is most
fully in the overall heterotrophic uptake unlikely that phytoplankton or zooplankand cycling of DOM. At the small concen- ton contributed significantly to the uptake
trations mentioned the low affinities of the process.
integumentary transport systems of aniIn order to investigate epidermal uptake
mals only enable an uptake proceeding at of dissolved amino acids in the sea star Assuch low rates that scarcely a substantial terias rubens, we used 10 fjM of a mixture
proportion of their metabolic needs is pro- composed in the relative, individual provided by the substances absorbed.
portions published for offshore waters of
With a few exceptions all animals are ca- the Baltic and the North Sea (Bohling,
pable of effectively processing particulate 1970, 1972; Dawson and Pritchard, 1978;
726
DIETRICH SIEBERS
r-10
10-1
c
o
-5
c
0)
o
c
o
o
0
0.5
1
1.5
2
Time (h)
2.5
3.5
FIG. 2. Asterias rubens. Net flux of a natural amino acid mixture (open squares) and glycine in the presence
(open circles) and absence (closed circles) of 20 mg liter"1 streptomycine sulfate. Controls were performed
with (open triangles) and without (closed triangles) the antibiotic. The number of replicates was n = 6, and
the weight-water relation 75 ml aerated "sea water of low bacterial activity" g~' (Siebers, 1979).
Siebers, 1979). The sea water used was taken from the German Bight. In the laboratory it had been aged in dark glass containers for months. Prior to use it was
filtered and aerated in a closed system in
absence of nutrients at dimmed light for
weeks. Due to these minimum conditions
it contained the unusually low number of
600 ml"1 bacteria, which were in a resting
state. With the unphysiological biomass/
water relation of 1 g body weight per 75
ml of this "sea water of low bacterial activity" (600 ml^1) rapid amino acid uptake by
the sea star was observed, decreasing within 4 hr the initially present level of 10 fxM
to about 4 fjM in the case of the amino
acid mixture and to 1.7 /x/Vf in the case of
glycine (Fig. 2) (Siebers, 1979). As can be
anticipated from the dormant state of the
bacterial populations, antibiotics had no
effects, and amino acid levels in controls,
containing no sea star, remained unchanged. Thus, the total uptake measured
must be contributed to the absorptive capacity of the sea star.
When, however, the biomass-water relation was changed to somewhat more realistic conditions of 1 g body weight per
liter of sea water, the reduction of amino
acid concentrations proceeded more slowly (Fig. 3), reaching levels of about 3.7 yM
within 30 hr. Notably, also in the controls
containing no sea star, amino acids decreased as a result of bacterial uptake,
which commenced after recognition of the
added substrates by the dormant bacterial
populations and induction of their uptake
systems. Recognition and induction belong
to the processes taking place within the initial lag period, during which no or onlysmall uptake is observed (Hollibaugh, 1979;
Siebers, unpublished). These findings indicate that the amino acid decreases observed in the ambient water of sea stars are
actually due to asteroid uptake plus microbial absorption. The proportion of the to-
727
BACTERIAL-INVERTEBRATE INTERACTIONS
10-
-10
5-
-5
12
30
48
36
Time (h)
55 158
57
53T
68
Fie. 3. Asterias rubens. Transepidermal net flux (closed circles) of 10 /AM amino acid mixture and concentration development in controls (open circles). The amino acid concentration was monitored, and after appropriate decreases filled up again to 10 /xM at 30, 38, 58, and 64 hr. The experiment was started with "sea
water of low bacterial activity" (n = 4) with a water-weight relation of 1 liter g"1 body weight (Siebers, 1979).
tal uptake, which can be attributed to integumentary transport by the sea star, is
enclosed by the two curves obtained for sea
stars and controls. This proportion of uptake by sea stars is reduced to zero levels,
when the decreased amino acid concentrations are filled up repeatedly, imitating the
natural complex processes of input. Due
to the adaptive bacterial life strategies,
based on induction and multiplication,
amino acid uptakes initially necessitating
30 hr, are performed within about 2 hr
after an experimental period of about 3 d,
during which bacterial densities have increased from 600 to about 2 x 106 ml"1.
We suggest that these results can be generalized to describe the competition in absorption of DOM between bacteria and
soft-bodied pelagic and epibenthic metazoans, which actually possess the capacity
to absorb nutritional solutes, but are totally
inferior to bacteria which are—in contrast
to the static animals—rapidly changing dynamic individual systems and populations.
The low total levels of about 0.1 fiM monosaccharides and 0.2 yM total amino acids
encountered in most offshore and many
coastal waters are most probably a result
of bacterial dynamics and uptake capacities.
BLOTURBATION AND FOOD RELATIONS
IN SEDIMENTS
To understand the driving forces ultimately underlying metabolic processes of
bacteria in all sediment depths, it is necessary to consider the role of macrofauna
and the close interrelations between microbial and animal existence. Macrofauna in
sediments exhibits considerable bioturbation activity, in terms of the processes of
vertical and horizontal translocation of
water and sediment components by the activity of larger metazoans. Sediment-dwelling deposit feeders provide themselves and
the life processes in deeper sediment layers with oxygen by pumping water through
their burrows. They feed on sediments and
many of them collect particulate detrital
sinks from the sediment surface, which are
thus conveyed into deeper layers (Hylleberg and Henriksen, 1980) (Figs. 4, 5).
DIETRICH SIEBERS
728
.
"
•
FIG. 4. Nereis diversicolor on its grazing area which
has partially left its burrow. (The photo was kindly
provided by Dr. Goerke, Bremerhaven, FRG.)
Since bacteria rely exclusively on dissolved nutrients, microbial degradation of
particulate detritus introduced by meta" i
zoans includes secretion of extracellular
enzymes and hydrolysis of solid substrates
to yield the low molecular weight organic FIG. 5. Nereis diversicolor, attracted by small pieces of
substances, which can be absorbed and me- soft parts of the bivalve Mytilus edulis. Note the cetabolized. In this way DOM is released to mented sand grains, visible in the upper part of the
the interstitial water phase, reaching con- burrow and the thin, light, oxygenated layer of the
surface and the halos alongside the burrow,
centrations often higher than in the water sediment
which contrast to the darker zones remote from the
column, and dissolved nutrients such as burrow. (The photo was kindly provided by Dr.
amino acids, carbohydrates and organic Goerke, Bremerhaven.)
acids become the most important intermediates in the cycling of organic matter
within detrital food chains.
As documented by J0rgensen (1980), the ergy and matter between the sediment and
presence of larger invertebrates, e.g., Ne- the water column.
reis virens and Corophium sp. in isolated sed- Striking correspondences in provision
iment cores increased sediment efflux of and cycling of nutrients exist between maprimary amines and bacterial uptake of rine sediments and terrestrial soils. With
glycine in the deeper sediment layers, ob- respect to worms Brinkhurst (1980) wrote:
viously due to sediment agitation and en- "The marine worms are to aquatic soils
hanced rates of nutrient distribution by what earthworms are to garden soils. They
water pumping.
irrigate, affecting the geochemistry of the
To continue the list of processes of bio- mud/water interface; they retrieve organic
turbation, release of metazoan faeces to the matter bound for incarceration in the sedsediment surfaces must be mentioned. Fil- iments; they maintain efficiency in bacteter feeders generate a stream of water rial populations and accumulate metals that
through various kinds of filtering devices can be exported through predation."
to obtain oxygen and to retain nutrient
And regarding the key role played by
particles, which are thus transferred from bacteria in the functioning of ecosystems,
the water column to the sediments. Hence, Fenchel and J0rgensen (1977) stated that
bioturbation acts as the motor of all met- many of the principles, derived from
abolic processes occurring in the sediment aquatic systems, apply equally well to terby permanently providing linkages of en- restrial systems, since all microorganisms
~
.
•
- «
BACTERIAL-INVERTEBRATE INTERACTIONS
729
require free water and in this sense are the textbook knowledge of the bacterial
aquatic organisms.
pathways indicated. However, the strongly
It is characteristic of the organismic re- interrelating contributions of the polylations prevailing in marine sediments that chaete can be listed: The worm introduces
the fauna creates all essential life condi- particulate organic carbon and nitrogen
tions including food supply for bacteria, after collecting and fragmenting detrital
while these in turn play an important role sinks on a defined grazing area of the sedin the nutrition of animals. Protozoa and iment surface. When the worms irrigate
the smallest metazoa, gastrotrichs and ro- their burrows, sea water of the water coltifers, mainly seem to feed on bacteria. umn is exchanged with water containing
Grazing on bacterial cells, slime layers, etc., dissolved sediment components, among
densely covering the surfaces of sand grains them dissolved organic substances, nitrate
and detritus particles, represents the ma- and hydrogen sulfide. Oxygen is introjor food supply for members of the meio- duced, and in addition sulfate as a signiffauna, among them turbellarians, nema- icant source of oxygen after reduction to
todes, oligochaetes, harpacticids and other sulfide. Furthermore, the polychaete exsmall Crustacea. Many of the larger meta- cretes ammonia and carbon dioxide.
zoans, among them polychaetes, snails,
Within this picture of integrated bacteamphipods and other members of the rial and animal life processes the question
crustacean macrofauna, ingest and me- can be raised whether metazoans do parchanically rework the whole complex of ticipate in uptake of dissolved organic matdetritus and microorganisms (Fenchel, ter at rates enabling them to satisfy a sig1970; Rhoads, 1974; Weise and Rheinhei- nificant proportion of their metabolic needs
mer, 1978; Meyer-Reil and Faubel, 1980). by the carbon and energy content of the
Gardening of digestible microorganisms ingested substances.
has been found in lugworms (Hylleberg,
In this context many previously per1975) and may potentially also occur in the formed experiments, which used a depolychaete, Capitella capitata (Hylleberg and fined, often small volume of sea water,
Henriksen, 1980). Free-drifting bacteria added dissolved organic nutrients, insertmay sometimes be too small to be retained ed a soft-bodied metazoan and monitored
by filter feeders, but bacteria adhering to net uptake in terms of concentration
particles represent a considerable source changes of the organic solute in relation to
of nutritional biomass.
time, have to be criticized. This experimental design may serve to analyze certain
HETEROTROPHIC UPTAKE IN SEDIMENTS
biochemical aspects of uptake, but is far
In sediments the carbon cycle, which is too simple to represent sediment condikept working by means of microbial activ- tions, because all influences from sediment
ity, reflects the fundamental metabolic structure are disregarded.
processes based on decomposition and exPolychaetes secrete mucus materials to
ploitation of dead organic material. Only cement the sand grains of the inner walls
the thin upper layer of marine sediments, of their burrows which thus provide firm
including the area of irrigated burrows, housings, protect their inhabitants from the
enables aerobic bacterial metabolism to oc- toxic properties of interstitial H2S and encur. Along with sediment depth, the hab- large the thin oxidized surface area of the
itat becomes anoxic. Here mineralization sediments by up to 100%. Irrigation uses
proceeds in a sequence of metabolic steps, water of the overlying water column which
often represented by different bacterial is circulated back to this location after
species using different nutritional sub- metazoan oxygen uptake. Hence, the instrates (Fenchel and J0rgensen, 1977). A terstitial water which may sometimes conscheme of the metabolic routes exhibited tain higher levels of DOM is scarcely availby bacteria is shown in Figure 6, together able to the polychaete. It must be assumed
with the burrow of a nereid polychaete. It that in relation to the amounts of water
is not intended here to refer in detail to irrigated in vertical directions, the amounts
OS
o
sulfur cycle
nitrogen cycle
electron
acceptors
400
CO,
-t> fixation
^absorption
DOM
C0 2
-absorption
ammonification
diffusion
amino acids, carbohydrates, fatty acids
organic acids
C02
refractory material
1
-100
methane
oxidation
sulphate
reduction
A
NH3/NH£ -oabsorption
oxigenoted
layer
En[mV]
lactate ,• succinate
malate
pyruvate
C02
S'-J
CH<
formate
acetate
methanol
FIG. 6. Scheme of the metabolic pathways of bacteria in sediments together with the burrow of a nereid
polychaete, showing the dependence of bacterial metabolism on macrofaunal activity. (The bacterial pathways
were modified and redrawn from Fenchel and J0rgensen, 1977.)
set
-200
C02
-300
n
BACTERIAL-INVERTEBRATE INTERACTIONS
731
r-15
|
| Meiofauna
of true interstitial water available to the
polychaetes as a result of horizontal water
I
1 Seston
movements is very small, and the percentages by which this water is depleted of
DOM by integumentary uptake are not
-10
10known. Polychaete burrows may be of considerable permanence. Kriiger (1964) reported that the lugworm, Arenicola marina,
inhabits its housings for weeks and months
-5
at the same location.
.i 5
Goerke (personal communication) inserted specimens of Nereis virens in
U-shaped glass tubes, which were sealed at
both ends except for a few small openings,
0J
less than 1 mm in diameter. These tubes
24 h
were placed in sediment areas of the German Bight. The polychaetes which had no FIG. 7. Distribution of label after incubation of sediment cores taken from a sandy wave-washed beach
or only little access to paniculate food ob- of
the Kiel Fjord (Baltic Sea, FRG) with tritiated gluviously could not rely on dissolved organic cose. M = Meiofauna, S = Seston, including bacteria
nutrients, since they rapidly lost body and detritus particles, liberated after several washings
weight. However, as Goerke mentioned, of the sediment by agitating with sea water (modified
they were able to produce paniculate faeces after Meyer-Reil and Faubel, 1980).
at the expense of body mass and by feeding on aufwuchs covering the inner walls
of the glass tubes or smaller paniculate de- densely inhabited by meiofauna, abiotic
tritus materials passing the the holes.
factors such as dissolved organic matter and
Directing our attention from the taxa of dissolved gases steadily diffuse between
macrofauna to members of small intersti- overlying oxic and oxygen-poor interstitial
tial meiofauna, including among others os- water. It can therefore be concluded that
tracods, copepods, annelids, nematodes, interstitial meiofauna is most probably not
gastrotrichs, turbellarians, and gnathosto- in contact with the higher levels of dismulids, we can see marked dependence of solved nutrients sometimes encountered in
all these forms on oxygen supply, as has detritus-rich sediments. It is questionable
been stated recently by Reise and Ax whether, in the meiofaunal habitats char(1979). These authors rejected the hypoth- acterized by diffusion of gasses and organesis of Fenchel and Riedl (1970) on the ex- ic nutrients this diffusional nutrient supply
istence of specific thiobiotic meiofaunal is sufficient to maintain nutrient concenforms adapted to the extreme habitat of trations in the direct vicinity of the integthe anaerobic sulfide-rich black sediment uments of the meiofauna at levels enabling
layers. In the studied area of a tidal flat epidermal uptake to proceed at rates senear the island of Sylt in the eastern part curing significant nutritional benefits.
of the North Sea, meiofauna was found
Meyer-Reil and Faubel (1980) incubated
consistently within the few millimeters of undisturbed sediment cores collected in
oxygenated surface layers of the sediments plastic tubes from wave-washed sandy
or in close proximity to the thin oxygen- beaches of the brackish-water of Kiel Fjord
ated halos alongside the oxic burrows of and Kiel Bight (Baltic Sea, FRG), where
the lugworm Arenicola marina. Remote from bacterial carbon was four times as high as
burrows, the anaerobic sediments more meiofaunal carbon, for 6, 12 and 24 hr
than 4 cm below the oxic layers were al- with low levels of tritiated glucose (Fig. 7).
most devoid of meiofauna.
Initially labeled glucose rapidly (6 hr) associated
with bacterial biomass and detriWithin the oxygenated aerobic/anaerobic interfaces of the sediment surface layer tus particles, and only small proportions of
and the burrow walls which are most tritium—about 1%—were detected in the
732
DIETRICH SIEBERS
serted in sea water depleted of amino acids
by means of various mechanical and char15
15coal filtering, ozonization and UV-irradiation, and subsequently enriched with low
concentrations of 0.1 and 0.3 yM of an
amino acid mixture. At higher levels of 0.8
i
-10
and 1.6 yM, net influx is observed. From
o 10these data, a concentration is calculated,
I
amounting to 0.5 yM, at which influx
equals efflux, thus resulting in unchanged
ambient concentration. Ferguson there•0 5
2 0 5fore suggests, that the real benefit of the
uptake mechanisms may be to prevent loss
of the body amino acid pools. It is interesting to note that the calculated equilibrium amino acid concentration of 0.5 yM,
0
0
30
10
20
at which influx equals efflux, is close to the
Time (mm)
level of 0.2 yM proposed as reasonable
FIG. 8. Changes in amino-acid concentrations of natural sea water concentration in a commedia (353 ml initial volume) produced by ten sea
stars of the genus Echinaster (77 g total weight) (mod- pilation of amino acid data by Dawson and
Pritchard (1978). The same explanation—
ified from Ferguson, 1980).
prevention of net losses of low molecular
weight body-own substances by means of
meiofauna. However, bacterial and detri- reabsorption of such molecules within the
tal radioactivity decreased greatly in the integument which are lost by diffusion
course of the experiments (12, 24 hr), through or between the epidermal cells—
whereas label in meiofauna increased, ob- is proposed by Gomme (1982) on the basis
viously as a result of grazing on bacteria. of findings on glucose fluxes in the polyThe authors therefore rejected the hy- chaete Nereis diversicolor.
pothesis that dissolved organics might represent a major direct nutrient supply for
REFERENCES
small infaunal invertebrates.
L
J
CONCLUSIONS
While still questioning whether transintegumentary absorption of DOM is quantitatively important in the nutrition of softbodied marine invertebrates, we shall
present a view on the biological significance of the uptake phenomena which are
observed by all workers. As argued by J0rgensen (1976) epidermal transport of small
organic molecules plays a minor role as a
source of energy in aquatic organisms, but
rather reflects a general property of the
membrane cell, a conclusion, which is also
consistent with the vestigial nature of the
transport systems. A reasonable role of the
uptake systems is suggested by Ferguson
(1980), who determined net fluxes of an
amino acid mixture in the sea star, Echinaster sp. As shown in Figure 8, net loss of
amino acids occurs when the sea star is in-
Bohling, H. 1970. Untersuchungen iiber frei geloste Aminosauren im Meerwasser. Mar. Biol.
6:213-225.
Bohling, H. 1972. Geloste Aminosauren in Oberflachenwasser de Nordsee bei Helgoland: Konzentrationsveranderungen im Sommer 1970.
Mar. Biol. 16:281-289.
Brinkhurst, R. O. 1980. Taxonomy, pollution and
the sludge worm. Mar. Poll. Bull. 11:248-251.
Dawson, R. and R. G. Pritchard. 1978. The determination of a-amino acids in sea water using a
fluorimetric analiser. Mar. Chem. 6:27—40.
Fenchel, T. 1970. Studies on the decomposition of
organic detritus derived from the turtle grass
Thalassia testvdinum. Limnol. Oceanogr. 15:14—20.
Fenchel, T. M. and B. B.j0rgensen. 1977. Detritus
food chains of aquatic ecosystems: The role of
bacteria. Advances in Microbial Ecology 1:1—58.
Fenchel, T. M. and R. J. Riedl. 1970. The sulfide
system: A new biotic community underneath the
oxidized layer of marine sand bottoms. Mar. Biol.
7:225-268.
Ferguson, J. C. 1980. Fluxes of dissolved amino
acids between sea water and Echinaster. Comp.
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