Download Role of Different Microbes and Substrates as

BULLETIN OF MARINE SCIENCE, 35(3): 283-298, 1984
ROLE OF DIFFERENT MICROBES AND SUBSTRATES
AS POTENTIAL SUPPLIERS OF SPECIFIC, ESSENTIAL
NUTRIENTS TO MARINE DETRITIVORES
Neal W Phillips
ABSTRACT
All animals must obtain (in addition to sources of energy and protein) certain specific
essential nutrients in order to survive, grow, and reproduce. Most research concerning the
nutrition of marine detritus feeders has focussed on caloric and protein needs, but requirements for certain specific nutrients, including essential fatty acids, sterols and essential amino
acids, have been defined in recent aquaculture research. This paper raises the question of
how marine detritus feeders are likely to obtain these required nutrients in their food. I argue
that the distribution of required specific nutrients in different components of the detrital
"trophic complex" is predictable, and that procurement of these nutrients could influence
feeding strategy. Bacteria, for example, lack long-chain linolenic (w3) series polyunsaturated
fatty acids (PUFA) that are essential in the diet of most marine metazoans; they also lack
sterols, which are essential for some invertebrates, including all crustaceans and some bivalves. Diatoms, in contrast, characteristically exhibit high proportions ofPUFA, especially
20:5w3, which should make them an excellent source of dietary essential fatty acids. Eukaryotic cells contain sterols, many of which can probably be converted to cholesterol (or
other characteristic forms) by marine invertebrates. Bacteria may be important as suppliers
of other specific essential nutrients, such as B-complex vitamins, and consumption of a mixed
diet including different microbes and substrates could help to remedy nutritional deficiencies
of specific detrital components (e.g., by protein complementarity). Studies ofthe nutritional
value of detritus and factors affecting trophic transfer in detritus food webs should explicitly
consider the importance of animal requirements for specific, essential nutrients as well as
energy and protein.
All animals must obtain (in addition to sources of energy and protein) certain
specific, essential nutrients in order to survive, grow, and reproduce. The purpose
of this paper is to raise the question of how marine detritus feeders are likely to
obtain these specific, essential nutrients in their natural diets. The problem is of
particular interest because many specific nutrient requirements of marine invertebrates have only recently been elucidated by research in aquaculture nutrition,
and because detritus feeders, unlike carnivores and selective herbivores, consume
foods that are typically heterogenous in biochemical composition. I argue that
the distribution of certain specific, essential nutrients among components of the
detrital trophic complex (Tenore and Rice, 1980)-including vascular plant, seaweed, and phytoplankton substrates, bacteria, fungi, protozoans and meiofaunais predictable, and that the need to insure the procurement of these nutrients may
influence feeding strategy. In addition, I suggest that some previous observations
concerning the trophic ecology of detritus feeders may reflect needs for essential
nutrients, and I identify areas of critical concern for future research.
The term detritus feeder encompasses an array of feeding types having in common the ingestion of some non-living particulate organic matter (Anderson and
Sedell, 1979; Tenore and Rice, 1980). Most research to date has necessarily
employed a simplified approach to the nutrition of detritus feeders, focussing on
the relative importance of microbial vs. plant substrate organic matter as energy
or protein sources (Newell, 1965; Fenchel, 1970; Hargrave, 1970; Lopez et al.,
1977; Cammen, 1980). Some recent work has sought to place the problem in a
283
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1984
more classical nutritional framework (Tenore, 1977; 1981; in press) by demonstrating that rations of nitrogen and "available" calories in detritus can predict
individual growth rates and population carrying capacity of deposit feeding polychaetes. However, little attention has been focussed on other nutritional differences among components of detritus, perhaps reflecting the tacit assumption that
minor nutritional requirements are of little consequence to the animals or that
these other nutrients are as likely to be obtained in one component of detritus as
another. An exceptional view was provided by Barlocher and Kendrick (1978),
who suggested that vitamins or other micronutrients in detrital microbes could
be responsible for the enhanced survival and growth of detritivores on microbialenriched detritus (although the authors did not provide any specific experimental
evidence). Cowley and Chrzanowski (1980) showed that inclusion of salt marsh
yeasts in B-complex deficient diets offered to deposit feeding fiddler crabs could
remedy the effects of the vitamin deficiency, but the significance of this result in
the context of the animals' natural diet is unknown.
ANIMAL NUTRITIONAL REQUIREMENTS
Nutritional requirements can be categorized as specific or non-specific. Specific
needs can only be satisfied by one (or one of a limited suite of) organic compound(s), whereas a variety of compounds can satisfy non-specific needs. For
example, animals have non-specific needs for reduced carbon (organic material),
which is catabolized to provide energy, and nitrogen, which is incorporated into
protein. Examples of specific nutrient needs include essential fatty acids, essential
amino acids, certain sterols, vitamins and other growth factors. Requirements for
some essential nutrients (e.g., essential amino acids) are fairly consistent across
the animal kingdom, whereas others vary depending on the particular taxonomic
or physiological group or developmental stage of the animal.
Most specific nutrient requirements have been elucidated for domestic animals
(McDonald et al., 1973; Church and Pond, 1974) and insects (Dadd, 1983). In
recent years, aquacultural research has defined many of the dietary requirements
(with the exception of some micronutrients) for a variety of fish (Cowey and
Sargent, 1979) and shellfish (Proder et al., 1983) of commercial importance. The
following sections provide a brief review of selected specific nutritional requirements that have been established for marine invertebrates, focussing on essential
fatty acids and essential amino acids (the reader is referred to Proder et al. [1983]
for more detailed information on nutritional requirements). As each nutritional
requirement is discussed, the distribution (if known) in the corresponding vascular
plant and seaweed substrates, bacteria, fungi, microalgae and protozoans, is described. These findings are combined to provide a preliminary evaluation of the
potential suitability of each component as a supplier of these essential nutrients
to marine detritus feeders.
Fatty Acids.-Lipids serve several important functions in metazoans: they are
important components of membranes and are involved in membrane transport
processes, are used as energy storage compounds, and function as metabolic regulators and hormones (Lehninger, 1975). Fatty acids· are aliphatic hydrocarbons
that are components of lipids, including triacylglycerols and phospholipids (Sargent, 1976).
, Fally acids are designated by the number of carbon atoms in the chain, the number of double bonds, and the position of the last
double bond in number of carbon atoms from the methyl end. Thus, 18:3w3 refers to an 18-carbon chain with three double bonds, the
last of which is located between the third and fourth carbon atoms from the methyl end.
PHILLIPS: DETRITIVORE
285
NUTRITION
Table I. Partial fatty acid spectrum of some marine animals, illustrating the typical marine pattern
in which the dominant polyunsaturated acids are 20:5w3 and 22:6w3. Values are given as the percent
of total fatty acids for each specimen. NR = not reported; (-) indicates not detected
Animal
Fatly acid
16:0
18:0
18:1w9
18:2w6
18:3w3
20:5w3
22:6w3
Nephtys
incisaa
;nfundibulumb
16.2
13.1
16.1
NR
NR
23.2
14.2
23.2
5.2
4.3
0.6
0.4
22.4
19.6
Bolinopsis
Peneaus
indic~
15.5
8.2
12.8
4.3
1.0
11.2
11.0
Calanus
helgolandieUS'
Crassostrea
gigas'
40.0
4.1
2.7
7.7
2.2
5.9
13.3
36.5
5.3
11.4
15.8
Fundulus
heteroclitld
9.0
5.1
10.0
1.6
2.7
7.5
28.6
• Deposit fceding polychaete. Fanington et at, 1973.
b Oenophore.
Monis et at. 1983. Phospholipid fraction only.
'Crustacean (prawn). Read, 1981. Animals fed "reference diet."
• Crustacean (zooplankter). Lee et a!., 1971. "Wild type" animals; phospholipid fraction only.
o Mollusc (oyster spat). Langdon and Waldock,
1981. Hatchery-reared spat; phospholipid fraction only.
'Salt marsh killifish. Jeffries. 1972. Muscle extract.
Marine invertebrates have a characteristic fatty acid pattern (Table 1) typified
by relatively high levels of two long-chain, polyunsaturated acids: 20:5w3 and 22:
6w3 (Farrington et aI., 1973; Sargent, 1976; Joseph, 1982). The relative proportions of particular fatty acids can differ among lipid classes and specific tissues or
organs within an animal, and may also differ depending on environmental variables such as temperature and salinity (Ackman, 1983; Castell, 1983). Nevertheless, the abundance of20:5w3 and 22:6w3 is a consistent feature of marine animals
with the major exception of hard corals, which generally contain low levels of
polyunsaturated fatty acids (Meyers et aI., 1978). Freshwater and terrestrial animals are characterized by higher levels of the linoleic (w6) series fatty acids (Castell,
1983).
Most metazoans can synthesize unbranched, even-length chains from acetate
and can desaturate at the ninth carbon from the carboxyl group (e.g., 18:0 -> 18:
lw9) (Sargent, 1976; Tinoco, 1982; Ackman, 1983; Castell, 1983), However,
further desaturations toward the methyl end of the chain (e.g., at the w3 position)
are either impossible or proceed very slowly; therefore, polyunsaturated fatty acids
(PUFA), especially those of the linolenic (w3) series, are required in the diet to
produce the 20:5w3 and 22:6w3 acids characteristic of marine invertebrates (Table
1). Although such needs can apparently be met to a limited extent by 18:3w3,
longer, more highly unsaturated acids such as 20:5w3 and 22:6w3 are much more
effective in promoting growth and normal metabolism (Jones et aI., 1979; Kanazawa et aI., 1979; Langdon and Waldock, 1981; Read, 1981). In some terrestrial
domestic animals, deficiencies in PUF A can result in decreased tissue PUF A
levels, impaired functioning of membranes and membrane-bound enzyme systems, reduced fertility, and other pathological conditions (Bishop, 1976). The
exact functions of PUFA such as 20:5w3 and 22:6w3 in fish and shellfish are
unknown, but in other animals they serve as hormone precursors and important
constituents of membrane phospholipids (Tinoco, 1982). Dietary PUFA deficiencies can produce reduced tissue PUFA levels and reduced growth in marine
invertebrates (Langdon and Waldock, 1981).
Different detrital substrates and microbes have different and predictable characteristic fatty acid patterns (Table 2). Vascular plants such as marshgrass (Spartina alterniflora) and turtlegrass (Thalassia testudinum) exhibit a typical terrestrial
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1984
Table 2. Partial fatty acid spectrum of some representative detrital substrates and microbes. Values
are given as percent of total fatty acids for each sample. (-) indicates not detected
Detrital component
Fatty acid
16:0
18:0
18:lw9
18:2w6
18:3w3
20:5w3
22:6w3
Marsh grass·
Marsh fungib
24.1
3.1
7.8
17.3
40.3
20.4
7.0
27.4
33.0
2.0
Sediment
bacteriae
22.0
6.7
0.2
Diatoms"
Seaweedc
Protozoans'
6.3
NR
10.1
14.3
23.8
0.8
16.1
4.0
5.6
6.0
1.0
5.3
10.8
2.5
1.5
NR
19.7
32.1
18.1
0.7
• Spartina alterniflora, stems and leaves. Schultz and Quinn, 1973. The percentage of 18:3w3 varies from 40 in October to about 8 in
April, with complementary changes in l8:1w9 and 18:2w6.
b Sphaerulina
pedicel/ala. Schultz and Quinn. 1973.
, Aerobic bacteria isolated from Loch Eil sediment. Parkes and Taylor. 1983.
d Skeletonema
costal urn. Lee et al .• 1971. Phospholipid fraction only.
, Laminaria pal/ida (kelp). frond portion. Velimirov. 1979.
r Nocliluca miliaris. Dikarev et al.. 1982.
pattern with significant levels of 18:3w3 but very low levels oflonger, more highly
unsaturated fatty acids (Maurer and Parker, 1967; Jeffries, 1972; Schultz and
Quinn, 1973). These substrates also contain generally low absolute lipid levels
(i.e., <5%; Maurer and Parker, 1967; Odum and de la Cruz, 1967) and therefore
do not constitute a very likely source of dietary essential fatty acids (EFA) for
detritivores. In contrast, algae (including macroalgae, phytoplankton, and sedimentary microalgae) generally contain higher overall lipid levels (e.g., 10-20%;
Lee et aI., 1971; Orcutt and Patterson, 1974) and are characterized by appreciable
proportions ofl8, 20 and 22-carbon PUFA(Erwin, 1973; Wood, 1974; Velimirov,
1979; Tenore and Jeffries, unpubI.) (Table 2). The characteristic fatty acids and
their relative proportions vary depending on the algal group. Green algae generally
have only 18:2 and 18:3 PUFA (Erwin, 1973; Wood, 1974). Diatoms, in contrast,
are notably high in 20:5w3 (Orcutt and Patterson, 1974; Sargent, 1976; Volkman
and Johns, 1977) and should therefore provide an excellent source of dietary EFA
for deposit feeders, many of which apparently selectively feed on such microalgae
(Wetzel, 1977; Robertson et aI., 1980; Lopez and Kofoed, 1980).
Bacteria can have a high lipid content (e.g., up to 40% of dry weight), but they
are conspicuously lacking in long-chain PUFA (Kates, 1964; Parker et aI., 1967;
Perry et aI., 1979; Parkes and Taylor, 1983). Instead, bacteria are distinguished
by a predominance of odd-chain length, branched, saturated or monounsaturated
acids that can serve to identify the bacterial contribution to sediment lipids (Perry
et aI., 1979; Parkes and Taylor, 1983) and can even be detected in animals that
consume bacteria (Cosper et aI., 1984). There is one report ofa marine bacterium
that appears to contain significant levels of an 18:4w6 acid (Johns et aI., 1977);
although this acid is of potential importance as a precursor of prostaglandins via
20:4w6 (arachidonic acid), the limited evidence available (for penaeid shrimp)
suggests that the rate of conversion to 20:4w6 is low (Lilly and Bottino, 1981).
Blue-green bacteria, although procaryotic, contain significant levels of PUF A
(Parker et aI., 1967). Most PUFA in marine sediments are attributable to diatoms
or other microalgae rather than bacteria (Volkman and Johns, 1977).
Fungi (including yeasts) can contain up to 30% of total fatty acids as 18:2w6,
but have very low proportions oflonger chain PUFA (Schultz and Quinn, 1973;
Weete, 1974; Teshima et aI., 1981). Thus, although fungi may provide a slightly
PHILLIPS: DETRITIVORE NUTRITION
287
better source of dietary EFA than bacteria, they do not appear to be a very good
source of (w3) acids, especially in comparison to microalgae.
Nematodes, which are ubiquitous and important members ofmeiofaunal communities (Coull and Bell, 1979), contain up to 30% lipid (dry weight), and the
most common unsaturated acid is 18:2w6 (Krusberg, 1971; Nicholas, 1975). However, most data are from non-marine (and especially parasitic) forms that may
differ in fatty acid composition from their marine counterparts. Nematodes are
apparently unique among metazoans in their ability to synthesize their own longchain PUFA from acetate (Krusberg, 1971; Nicholas, 1975), which could make
them an important link in the detrital food web if they were consumed by macroinvertebrates in sufficient quantities. Their importance also depends on whether
the marine forms have (w3) acids as the predominant PUFA; no data are available
at present to evaluate this likelihood. A similar problem applies to marine protozoans. Most freshwater protozoans can generally synthesize long-chain PUFA
from simple precursors (Dewey, 1967), but data are lacking on marine forms.
Most data concerning fatty acid composition have been obtained from phytoflagellates, which exhibit a characteristic marine pattern with high levels of 20:5w3
and 22:6w3 (Holz, 1969; Dikarev et a1., 1982). However, heterotrophic protozoans
may not have the same biosynthetic capabilities as do the phytoflagellates. In
contrast to nematodes and protozoans, rotifers apparently cannot synthesize their
own PUFA (Teshima et al., 1981). With bacteria so clearly lacking in PUFA, any
protozoans and meiofauna that could consume bacteria and produce PUF A should
be a valuable food source for macroinvertebrates. Data concerning the fatty acid
composition and biosynthetic capabilities of marine protozoans and meiofauna
are critically needed in order to evaluate this possibility.
Because marine invertebrate tissue has such a characteristic fatty acid pattern
and high lipid levels (e.g., 10-30% for crustacean zooplankton; Lee et a1., 1971),
it should serve as an excellent source of dietary EFA for other marine invertebrates.
Aging Effects. - Research has documented gross changes in the nutritional value
of detritus with microbial aging (Odum and de la Cruz, 1967; Gosselink and
Kirby, 1974; Haines and Hanson, 1979; Rice and Tenore, 1981). Most work has
described changes in organic content and protein levels. However, changes in fatty
acid patterns of detrital substrates can be expected on a priori grounds and have
been demonstrated for some substrates. Generally, as decomposition proceeds,
energy-rich long-chain PUFA are rapidly broken down to more saturated, shortchain acids that are more characteristic of the bacteria and fungi involved in
decomposition (Schultz and Quinn, 1973); vertical profiles of fatty acids in sediment cores (Farrington and Quinn, 1973; Johnson and Calder, 1973; Van Vleet
and Quinn, 1979) and depth profiles of material deposited in sediment traps in
the open ocean (De Baar et al., 1983) reflect increasing proportions of saturated
fatty acids with depth (a correlate of increasing decomposition time). Thus, one
may expect substrates that are originally high in PUFA, such as phytoplankton
or seaweed detritus, or sediment microalgae, to decrease in suitability as dietary
EFA sources as decomposition proceeds. The net effect on the likely nutritional
value of vascular plant substrates is unclear; although these tissues usually contain
significant levels of PUF A when freshly dead (Schultz and Quinn, 1973), the
availability of vascular plant organic matter to macroconsumers is often low
(Tenore, 1981; in press).
CONCLUSIONS.
Marine invertebrates have a characteristic fatty acid pattern and
limited capabilities for synthesis of long-chain polyunsaturated fatty acids. Different components of the detrital trophic complex are likely to have predictable
288
BULLETIN OF MARINE SCIENCE, VOL. 35, NO.3,
1984
Table 3. Essential amino acid levels as percentages of total amino acids for a variety of marine
invertebrates
Animal
Composite
Amino
acid
THR
VAL
MET
ILEU
LEU
PHE
HIS
LYS
TRYP
ARG
crab'
Red
abaloneb
6,1
6.7
2.2
S.2
7.5
7.4
2.5
4.9
5.6
6.0
2.6
4.4
8.7
3.9
2.0
6.0
NR
NR
S.O
6.6
Dungeness
Euphausiidc
4.8
5.2
3.2
S.2
7.8
6.5
2.2
7.8
1.6
6.0
Tunicat""
Hard
corale
Sea
urchin'
5.3
5.4
2.4
4.6
7.3
4.8
2.6
7.6
5.0
4.6
2.1
3.7
5.9
3.8
2.6
9.70
4.1
4.2
0.7"
4.2
6.7
4.2
0.3"
5.8
NR
NR
NR
8.5
7.1
8.8
marine
invertebrate
5.2
S.4
2.S
4.6
7.3
5.1
2.4
6.4
1.6
7.0
• Cancer magister. Lasser and Allen, 1976 .
• Haliotus ruJescens. Allen and Kil8ore. 1975.
, Euphausia paci]i£a. Suyama et al., 1965.
cl
Pyrosoma sp. Raymont et al., 1975.
, Caryophyllia smithii. Raymont et .1., 1975.
, Strongylocentrotus droebachiensis. Fong and Mann, 1980. Values are approximate
animals.
I Value not included in calculations
for composite marine invertebrate.
averages over one year of field collections of the
fatty acid patterns and to vary in suitability as dietary EFA sources. Specifically,
fungi and (especially) bacteria appear to be poor sources; algae (especially diatoms)
are likely to be good sources; and animal tissue (e.g., animal carcasses) is likely
to be an excellent dietary EFA source. Protozoans and some meiofauna (nematodes) have the potential to serve as important intermediaries in detrital food
chains because they can synthesize PUFA, which are lacking in bacteria; however,
there is a critical need for specific data concerning the fatty acid composition and
biosynthetic capabilities of marine species. Detrital aging (microbial decomposition) should result in a rapid decline in levels of long-chain PUFA; this emphasizes the potential importance of fresh detritus, especially that derived from
labile sources such as phytoplankton or macroalgae that have initially high levels
ofPUFA.
Amino Acids.-Amino acids, as components of proteins, are necessary in the
production of enzymes and structural materials within animals; in addition, free
amino acids may function in osmoregulatory roles. Of the 20 amino acids commonly found in animal proteins, in general 10 can be synthesized from simple
precursors and the remaining 10 must be obtained in the diet. The latter are
termed essential amino acids (EAA). Marine invertebrates apparently have the
same EAA acid requirements as most of the animal kingdom. The essential amino
acids are: threonine (THR), valine (VAL), methionine (MET), isoleucine (ILEU),
leucine (LEU), phenylalanine (PHE), histidine (HIS), tryptophan (TR YP), lysine
(LYS) and arginine (ARG) (Dadd, 1983; Allen and Kilgore, 1975; Lasser and
Allen, 1976).
Marine invertebrates exhibit a fairly consistent distribution of essential amino
acids (percentage of total amino acids) in their tissues (Table 3) (Raymont et al.,
1975; Allen and Kilgore, 1975; Lasser and Allen, 1976). To produce tissue of this
composition, essential amino acids must be obtained in the diet in roughly the
same relative proportions that they occur in the animal tissues (Phillips and
Brockway, 1956; Cowey and Tacon, 1983). The suitability of a given food as a
protein source has commonly been evaluated by comparing the essential amino
PHILLIPS: DETRITIVORE
289
NUTRITION
Table 4. Relative deficiencies or excesses of essential amino acids (EAA) in various foods, in comparison to the tissue EAA profile of a composite marine invertebrate (see Table 3). Percent deficiency
was calculated as [(Cr - CJ/(CJ] x 100, where Cr is the percentage of the particular EAA in food
(percent of total amino acids) and C. is the same for animal tissue (Fong and Mann, 1980). Negative
values indicate deficiencies and positive values indicate excesses of each EAA. The four most deficient
EAA are listed below each column
Polential food
Amino
acid
THR
VAL
MET
ILEU
LEU
PHE
HIS
LYS
ARG
Live
eelgrass·
Dead
eelgrassb
Eelgrass
detritus.::
Green
seaweedd
17.6
33.3
-32.0
23.9
31.5
23.5
-33.3
-37.5
-50.0
ARG
LYS
HIS
MET
21.6
29.6
-44.0
23.9
26.0
11.8
-41.7
-32.8
-40.0
MET
HIS
ARG
LYS
13.7
46.3
-36.0
4.4
1.4
-5.9
-8.3
-6.2
-24.3
MET
ARG
HIS
LYS
15.7
14.8
36.0
8.7
6.8
2.0
-45.8
-20.3
-11.4
HIS
LYS
ARG
Microalgae'
5.9
-25.9
-12.0
-10.9
26.0
15.7
-45.8
7.8
-21.4
HIS
VAL
ARG
MET
Fungif
3.1
-8.3
-58.0
-11.3
-8.4
-41.2
45.8
58.8
66.3
MET
PHE
ILEU
LEU
Estuarine
particulale
materialH
3.8
14.8
-8.0
8.7
23.3
21.6
29.2
-9.4
-14.3
ARG
LYS
MET
•• ' Zostera marina. Thayer el aI., 1977.
d Viva lactuca (sea le\luce). Munda and Gubensek,
1976 .
• 25 species of phytoplanklonic algae. Chuecas and Riley, 1969.
r Single-cell prolein from Candida sp. (an alkane yeasl). Mahnken el aI., 1980 .
• Particulale malerial (>40 I'm) from Chesapeake Bay near mouth of the Paluxenl River (Sigleo el aI., 1983).
acid profiles of food and animal tissue (Burkholder et aI., 1971; Fong and Mann,
1980; Deshimaru, 1983). Theoretically, the EAA that is most deficient relative
to animal tissue will be limiting to growth. However, it has proven difficult to
demonstrate any dramatic effects of EAA deficiencies in several marine invertebrates (Armitage et aI., 1977; Fong and Mann, 1980; Carefoot, 1981). This is in
part due to compensatory mechanisms that apparently limit degradation of EAA
already present in tissues (Armitage et aI., 1977). Also, gut microbes could potentially supply some of the essentials lacking in the food (Fong and Mann, 1980),
as they can in domestic ruminants (Garrigus, 1970; Purser, 1970).
Although the potential effects of EAA deficiencies in marine invertebrates are
therefore not well established, it is instructive to examine the EAA profiles of
some potential detrital food sources (Table 4). Although no clear trend emerges
in terms of relative suitability of foods, it appears that certain amino acids are
most likely to be deficient, including the sulfur-containing MET and the basic
amino acids HIS, LYS, and ARG. The results are similar to those of Burkholder
et ai. (1971), who judged several species of seaweeds deficient in MET, LYS, HIS
and TRYP in comparison to fish tissue. Fong and Mann (1980) found that ARG,
MET and LYS were the EAA most likely to be limiting for sea urchins feeding
on kelp.
Bacteria and fungi are often considered to be deficient in MET when used as
the sole protein source for domestic animals (Miller, 1968; Bressani, 1968; Spicer,
1972) (Table 4 for example). Dabrowski et ai. (1980) also noted deficiencies in
ARG, LYS, and HIS in fish tissues as the proportion of fungal protein in their
diet was increased.
Most foods that a detritus feeder might encounter (with the exception of animal
tissue, which should be an excellent EAA source) are likely to be somewhat
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BULLETIN OF MARINE SCIENCE, VOL. 35, NO.3, 1984
deficient in one or more essential amino acids. Part of the problem could be
overcome by consumption of a mixture of foods, resulting in protein complementarity (McDonald et a1., 1973; Deshimaru, 1983). Also, as noted above, enteric
microbes could potentially supply some EAAs. The EAA profile of rumen microbes is usually not ideal, but the net effect of these microbes is to enhance the
protein value of a food having a poor EAA profile and to detract from the value
of one having a good profile (Garrigus, 1970). However, because certain essential
amino acids appear to consistently have the greatest potential for dietary deficiency, attention should be focussed on the potential for nutritional effects of
specific essential amino acid deficiencies in detritus. If certain essential amino
acids are consistently in short supply, the overall controlling influence of detrital
protein levels on detritivore growth and production (Tenore, 1981; in press) may
be due in part to limiting essential amino acids rather than protein per se. The
basic amino acids ARG, LYS and HIS, and the sulfur-containing MET, appear
to have the most potential for limiting detritivore growth.
Other Nutrients and Growth Factors.-A variety of other nutrients are generally
required in complete balanced diets for marine invertebrates, including sterols,
certain phospholipids, vitamins, minerals and other growth factors (D'Abramo
and Baum, 1981; Conklin, 1983). These requirements also have the potential to
influence feeding strategies, although the likelihood is more difficult to evaluate
than for nutrients such as essential amino acids and essential fatty acids. A few
examples are discussed below.
Some marine invertebrates (including all crustaceans and many bivalves) have
obligate dietary sterol requirements, and the absence of dietary sterols can produce
dramatic effects on crustacean survival (Teshima, 1983). The predominant crustacean sterol, cholesterol, is a precursor of a and fJ ecdysones (molting hormones)
(Pennock, 1977), and animals fed sterol-deficient diets exhibit a characteristic
molt-death syndrome (Teshima et a1., 1983); the syndrome can also be generated
by a deficiency of dietary phosphatidylcholine, which is involved in cholesterol
transport in the hemolymph (D'Abramo et a1., 1982). Eukaryotic cells generally
contain sterols at about 1% of dry tissue weight (Goodwin, 1973), but bacteria
are considered not to contain sterols (Lehninger, 1975; Lee et a1., 1980). However,
the particular variety of sterols characteristic of different eukaryotic phylogenetic
groups varies widely (Goad, 1976; Morris and Culkin, 1977), and the relative
capacities of marine invertebrate consumers (such as detritus feeders) for conversion of dietary sterols for their own use is not well known. Prawns can convert
a variety of sterols (including ergosterol, a characteristic fungal sterol) to cholesterol (Teshima et a1., 1983).
Cowley and Chrzanowski (1980) showed that inclusion of salt marsh yeasts in
prepared, B-complex vitamin deficient diets offered to deposit feeding fiddler crabs
could remedy the effects of the vitamin deficiency. The B-complex vitamins are
involved in intermediary metabolism and deficiencies are therefore likely to have
serious effects on growth and/or surviva1. However, dietary requirements for these
vitamins are likely to be low, and there are several potential sources, including
bacteria (Kutsky, 1981), yeasts (Cowley and Chrzanowski, 1980), phytoplankton
and other algae (Carlucci and Bowes, 1971), vascular plant tissue (Burkholder,
1957) and ambient water and sediments (Maurer and Parker, 1968).
The potential importance of dietary micronutrient requirements in the nutrition
of marine detritus feeders cannot be established on the basis of information
presently available. However, because a variety of these micronutrients have
critical metabolic roles, their significance should be investigated as more infor-
PHILLIPS: DETRITIVORE NUTRITION
mation becomes available on dietary requirements
chemical composition of detrital components.
291
of detritus feeders and bio-
DISCUSSION
The emphasis of the preceding sections has been on detailing specific essential
nutrient requirements and comparing potential food sources as suppliers of those
nutrients. The focus on minor nutrients is not intended to deemphasize the importance of bulk requirements for calories and protein (Tenore, 1981; in press).
However, it is clear that marine invertebrates have some very specific nutritional
requirements and that these have a large potential for influence on fitness through
effects on survival, growth and reproduction. Because detritus is frequently composed of material that is derived from a variety of sources and that differs in
biochemical composition, the acquisition of the proper nutrients in suitable relative proportions is not a trivial concern. The extent to which deficiencies are not
observed or noticed in nature (as evidenced by, for example, the consistency of
EFA and EAA patterns in marine invertebrate tissues, as cited above) may reflect
feeding adaptations of the animals to insure proper nutrient uptake.
Some of the results discussed above are in accord with known research findings
on the trophic ecology of detritivores, whereas others are difficult to explain. For
example, bacteria appear to be a poor primary food source because they lack
PUFA and sterols; fungi appear to be somewhat more nutritious, having ergosterol
and low levels of PUFA. Research using freshwater animals has demonstrated
that fungi are generally suitable food sources for detritivores (Kostalos and Seymour, 1976; Rossi and Fano, 1979; Willoughby and Marcus, 1979) and probably
better than bacteria as food (Kostalos and Seymour, 1976). However, fungi appear
more likely to be a suitable dietary EFA source for freshwater than marine detritus
feeders because the former are more likely to require or utilize linoleic (w6) series
acids rather than linolenic (w3) series acids, (Castell, 1983; Dadd, 1983); fungi are
likely to have significant proportions of 18:2w6 but not 18:3w3 and other (w3)
acids (Schultz and Quinn, 1973; Weete, 1974). Feeding studies using fungal diets
for marine detritus feeders are few; Gessner (cited in Kohlmeyer and Kohlmeyer,
1979, p. 153) has maintained
marsh amphipods on exclusive fungal diets for up
to several months, and grazing experiments with closely related species (Morrison
and White, 1980; Smith et aI., 1982) suggest that fungal biomass could be a major
food source for these organisms. There is an emerging consensus that bacteria are
not likely to be a primary energy source for macroinvertebrate detritivores because
the abundance of bacteria associated with detritus or sediment usually accounts
for a relatively small fraction of total organic carbon and nitrogen (Christian and
Wetzel, 1978; Rublee, 1982) and animals generally do not consume bacteria
associated with detritus or sediment rapidly enough to meet their energetic requirements for maintenance and growth (Cam men, 1980). In addition, it has been
pointed out that labile organic matter (i.e., material other than cellulose, lignin,
and xylan) is likely to be present in detrital substrates and to constitute a significant
energy and protein source even if assimilated far less efficiently than bacteria
(Baker and Bradnam, 1976; Bowen, 1980; Cammen, 1980). As pointed out earlier,
freshly deposited labile organic matter (e.g., from phytoplankton blooms or seaweeds) is likely to be of direct value as a source of dietary EFA. Bacterial extracellular organic matter, which is often more abundant than living bacterial biomass
in sediments or detritus (Paerl, 1978; DeFlaun and Mayer, 1983), has been proposed as a more likely food source for detritivores (Hobbie and Lee, 1980).
However, the material is generally composed of acid mucopolysaccharides (Paerl,
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BULLETIN OF MARINE SCIENCE, VOL 35, NO.3,
1984
1975; Hobbie and Lee, 1980) and is therefore not a likely source of dietary essential
fatty acids.
Most evidence for the relative importance of bacteria in detritivore diets has
been inferential, relying on information concerning relative abundance and relative assimilability of different microbes and substrates (Hargrave, 1970; Lopez
et a1., 1977; Cam men, 1980). However, some experiments have been conducted
to determine the suitability of bacterial diets for marine macroinvertebrates and
meiofauna. Given the apparent poor nutritional quality of bacteria as discussed
above, it is difficult to explain the apparent reliance on a bacterial diet by some
harpacticoid copepods (which, though meiofaunal, are crustaceans and should
have similar physiology to the larger forms) and nematodes, and the limited
evidence for success in raising some other marine invertebrates on bacterial diets
(Zobell and Feltham, 1938). Several experiments have demonstrated cope pod or
nematode survival and/or growth on bacterial diets (Rieper, 1978; Klekowski et
a1., 1979; Alongi and Tietjen, 1980; Ustach, 1982), and other research has implicated the relative importance of bacteria as a food source for these organisms
(Brown and Sibert, 1977; Rieper, 1982; Ustach, 1982). Caution must be exercised
in interpreting the results of such experiments, however. For example, rarely are
the animals cultured through several generations, when long-range effects may
become evident. Further, the chance of protozoan (Rieper and Flotow, 1981) or
blue-green algal contamination of the bacterial cultures must be carefully evaluated
because the nutritional characteristics of these organisms are quite different from
those of bacteria. Finally, it is not known whether the biochemical composition
of animals cultured on bacterial diets is comparable to that of animals in the field.
If it is not, this would indicate that inclusion of dietary items other than bacteria
is common (or perhaps necessary) in the natural environment. It would be overly
simplistic to conclude that because they lack PUFA and sterols, bacteria are not
a potentially important food source for some animals. Metazoans that obtain most
of their caloric and protein requirements by eating bacteria may need to have
feeding strategies that insure the consumption of some other food items to provide
certain essential nutrients. In addition, even if bacteria are unlikely to be a primary
source of calories for macroinvertebrate detritivores (as discussed above), they
could still be important sources of other specific essential nutrients such as EAA
or B-complex vitamins in the same sense that rumen microbes contribute some
essential nutrients to their hosts (Purser, 1970).
Because bacteria do not contain sterols and are lacking in PUF A whereas protozoans are not, the latter could serve as important intermediaries in detrital food
webs. The potential importance of protozoans as trophic links has already been
raised for freshwater (Porter et al., 1979), and marine (Pomeroy, 1974) systems.
To evaluate this possibility, data are needed concerning the fatty acid composition
and biosynthetic capabilities of heterotrophic marine protozoans and ubiquitous
meiofauna such as nematodes.
Microalgae (especially diatoms) appear to be an excellent food source, especially
from the standpoint of dietary EF A. Of course, such microalgae are also high in
nitrogen and labile calories (Tenore, in press). My review provides an additional
explanation for the predominance of selective deposit feeders that rely primarily
on a microalgal diet (Hargrave, 1970; Wetzel, 1977; Lopez and Kofoed, 1980;
Robertson et a1., 1980).
Animal tissue is likely to provide the most nutritious food source for a marine
invertebrate, both from the standpoint of energy/protein and essential nutrient
requirements. Animals that are not adapted for camivory can take advantage of
this by consuming fresh carcasses when they become available; such scavenging
PHILLIPS: DETRITIYORE NUTRITION
293
behavior is highly developed among deep-sea amphipods, for example (Smith
and Baldwin, 1982). Curtis and Hurd (1981) argued that cyclical regeneration of
the crystalline style in mud snails (Ilynassa obsoleta) constitutes a strategy to
insure the consumption of some animal tissue in the diet of these deposit feeders.
Because of the involvement oflipids in reproductive processes, one would expect
requirements for essential fatty acids to be most critical for reproductive females,
whereas protein and essential amino acid requirements are likely to be more
critical for rapidly growing juveniles. In either case, feeding behavior that results
in the inclusion of animal tissue in the diet should be highly advantageous for
detritivores.
Some caveats concerning the present analysis are in order. First, most of the
nutritional biochemistry for marine invertebrates has been derived from relatively
few species of commercially valuable fish and shellfish, some of which are detritus
feeders and some not. Although there are some nearly universal trends (e.g.,
essential amino acid requirements, inability of metazoans to synthesize PUFA
de novo) one should not rule out exceptions without further research. Second,
animal nutritional requirements should properly be evaluated by determining
rates of uptake and utilization, whereas the discussion in this paper has concerned
the percentage composition of dietary components. In theory, an animal could
obtain enough of a nutrient in short supply in the food by simply consuming the
food more rapidly than one in which the nutrient was relatively concentrated.
Many animals apparently compensate for the diluteness of energy and/or protein
in their food by increasing their ingestion rate (Mercer et al., 1981; Phillips,
1984), but they apparently do not similarly compensate for specific nutrient deficiencies (Cowey and Tacon, 1983), probably because compensation for low
dietary levels of particular micronutrients can result in excessive intake of others.
The suitability of different dietary components as sources of essential nutrients
such as EFA and EAA is commonly evaluated by offering animals isocaloric or
isonitrogenous diets differing in the spectrum of essential fatty acids or amino
acids (Read, 1981; Deshimaru, 1983). Therefore, it is likely that large differences
in relative proportions of essential fatty acids and amino acids in components of
detritus can have measurable effects on growth and/or survival of the animals.
This possibility can and should be investigated by several approaches. For example, natural food items (e.g., microalgae, particulate organic matter, etc.) could
be supplemented with essential fatty acids (and isocaloric additions of non-essential fatty acids as controls) to determine whether the concentrations of these
nutrients in the diet could be considered limiting. Alternatively, detritivores could
be fed prepared, defined diets deficient in particular nutrients and supplemented
with extracts or homogenates of natural food items; this is the approach used by
Cowley and Chrzanowski (1980) to demonstrate that salt marsh yeasts can supply
B-complex vitamins to deposit feeding fiddler crabs. These types of experimental
approaches are now feasible because of recent advances in the development of
microencapsulation techniques that allow defined diets or specific nutrients to be
supplied at known rations under controlled conditions (Langdon, 1983; Levine
et al., 1983). Finally, one could analyze field-collected animals and food items to
determine whether there is any correlation between food and tissue fatty acid
concentration; relationships between tissue composition and growth, survival,
and reproductive potential could be determined by laboratory experimentation.
Most research on the relative importance of microbes vs. substrates as food
sources for detritus feeders has relied on evidence concerning the relative abundance and assimilability of those foods. Future research should also consider the
importance of overall nutritional quality of the organic matter and the known
294
BULLETIN OF MARINE SCIENCE, VOL. 35, NO.3.
1984
nutritional requirements of marine animals. In order to define the roles of different
microbes and substrates as nutritional sources for detritus feeders, research is
needed on the biochemical characteristics of different detrital substrates and microbes and the physiological biochemistry of detritus feeding animals. The explicit
consideration of the specific nutritional requirements of detritus feeders can provide new and valuable insights into the functioning of detritus-based systems.
ACKNOWLEDGMENTS
This research was supported in part by NSF Grant OCE-82-00385 to K. R. Tenore. I thank C. J.
Langdon and an anonymous reviewer for helpful comments on the manuscript.
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DATEACCEPTED: June II, 1984.
ADDRESS: Skidaway Institute of Oceanography, P. O. Box 13687. Savannah, Georgia 314 I 6; PRESENT
ADDRESS: Continental Shelf Associates, Inc., P.O. Box 3609. Tequesta, Florida 33458.