Limnol. Oceanogr., 33(4, part 2), 1988, 946-962
Q 1988, by the American
Society of Limnology
and Oceanography,
Inc.
Comparative ecology of the macrofauna of freshwater and marine muds’
Glenn R. Lopez
Marine Sciences Research Center, State University
of New York, Stony Brook,
11794
Abstract
There are many striking similarities between the benthic macrofauna inhabiting marine and
lacustrine sediments. Most of the same trophic/functional
groups are well represented in both
habitats. There is no obvious difference between the tylpes of particulate food sources available for
microphagous animals. Temperate lakes and neritic environments support a similar standing stock
of macrofauna, which is a function of similar detrital input to the benthos. There is no characteristic
difference in P : B ratios between marine and freshwater macrobenthos. Predation and competition
have similar important efrects on community structure. Likewise, community succession appears
to follow the same pattern.
There are certain differences between marine and freshwater macrobenthos, however, that appear
to relate to fundamental habitat differences. The major #difference is that low salinity and the closed,
ephemeral nature or most lakes have resulted in little taxonomic similarity between the two faunas.
Tentaculate deposit feeders are found only in marine sediments, and interstitial suspension feeders
are common only in fi-cshwatcr muds. The ability to use dissolved organic matter is well developed
only in marine animals, which is a consequence of the osmotic problems faced by freshwater
animals. The ability of many limnetic species to survive prolonged anoxia relates to the lack of
tidal mixing in lak&.
This review is focused on how certain
fundamental differences between lacustrine
and neritic habitats control the behavior of
benthic organisms and the organization of
benthic communities. The most obvious differences are the discrete or closed nature of
lakes compared to the ocean, the eurytopic
condition of lakes, the ionic concentration
and composition of the waters, tidal currents, and the habitat lifespan. It is the purpose of this review to determine whether
these fundamental habitat differences manifest themselves in differences in the distribution of particular taxonomic, trophic, or
functional
groups, reproductive
and dispersal mechanisms, biomass and production, and response of individuals and communities to perturbations.
I restrict this comparison to the macrofauna inhabiting muds of lakes and coastal
marine environments.
Most examples are
taken from relatively well-studied
North
American and European lacustrine and shelf
habitats, although examples from estuaries,
rivers, saline lakes, ancient lakes, and brackish bays provide interesting perspectives on
some of the problems examined.
-’ Contribution
No. 606 from the Marine Sciences
Research Center, State University of New York, Stony
Brook.
946
IBecause muds are soft, most animals live
buried in the sediment. Animals living in
muds face the problems of initial recruitment into the appropriate substrate, limited
access to dissolved oxygen, and the difficulty of maintaining a stable living position
to collect food. The granulometric and mass
properties of lake and marine muds are
similar, although lacustrine sediments at a
given depth are typically finer grained than
miarine sediments because of the lack of tidal currents and higher sedimentation rates
(McCall and Tevesz 1982).
Discussions with D. Capone, L. Duguay,
R. Elmgren, I. Holopainen, L. Kofoed, and
J. Levinton were helpful in the development
of this manuscript. Reviews by D. Boesch,
J. Kelly, and J. Frithsen resulted in substantial improvements.
The fauna
Taxonomic groups-The
faunas of mari:ne and freshwater sediments are similar at
thie level of phyla, both being characteristically dominated by annelids, arthropods,
and molluscs. However, each phylum is
represented by different classes in marine
and lacustrine habitats.
In lacustrine muds annelids are represented by tubificid and naidid oligochaetes
and by leeches, arthropods by insect larvae
Benlhic macrofauna
and a few crustaceans, and molluscs by
sphaericean and unionid bivalves. Chironomids and oligochaetes dominate the biomass of most freshwater muds.
Oligochaetes are mostly small deposit
feeders that can dominate organically rich
sediments and are very resistant to anoxia.
Their densities can surpass 200,000 mm2.
Leeches are predacious and less tolerant of
anoxia.
Insects are well represented in lacustrine
sediments, but mostly as larvae (Hutchinson 198 1). The dipteran family of chironomids is the most important family; the
adults are never aquatic, and the larval stage
can last several weeks to >2 yr. This very
diverse group includes deposit feeders, suspension feeders, browsers, and carnivores,
and they often dominate the biomass, production, and diversity in lake muds. Another
dipteran family is represented by the phantom midge Chaoborus, which is a dominant
predator on zooplankton and zoobenthos in
many lakes.
Amphipods are the most important crustacean order in lake muds. Most of them,
except for Pontoporeia, are epibenthic omnivores that require aerobic conditions.
Pontoporeia is exceptional among amphipods in its nightly vertical migrations into
the water column: it is a burrowing deposit
feeder. Freshwater species of Pontoporeia
are glacial relicts of marine species and are
restricted to cold lakes. Another glacial relict is the mysid Lysis relicta, which is an
important nocturnal zooplankton predator
in cold lakes. Crayfish are among the largest
animals found in freshwater benthos; they
can dominate the benthic biomass in many
lakes.
Corbiculacean bivalves are cosmopolitan, ubiquitous, and typically prominent in
freshwater benthos. They are usually small,
and Pisidium spp. are strikingly so, with
most species attaining a maximum size of
< 1 cm. They are active burrowers and generally rather slow growing. The larger corbiculaceans,
including
Corbicula and
Sphaerium, are burrowing suspension feeders. The unionid bivalves are much larger
and are among the most conspicuous members of benthic macrofauna. Due to their
large size, they can dominate macrobenthic
947
biomass, but due to their longevity, their
production is generally low. These suspension feeders have an unusual pattern involving the production of larvae that are
parasitic on fish.
The fauna of marine sediments is more
difficult to describe in general terms because
more phyla are well represented, and there
is more diversity within each phylum. The
polychaetes are very diverse and are often
the single most important group in marine
muds. Many species are deposit feeders, but
all trophic types are represented. Pericarid
and decapod crustaceans are important arthropods in marine sediments. Insects are
rare and restricted to the intertidal zone.
Marine bivalves are also highly diverse and
often dominant members of marine muds.
Most are suspension or deposit feeders.
Salinity is the major environmental factor
restricting the distribution
of marine and
lacustrine taxa, resulting in the well-known
poverty of species in brackish (3-S%O) water
(Remane and Schlieper 197 1). Most marine
animals are restricted to the narrow range
of high salinity, but freshwater animals occur in a wide range of dilute salinities.
Therefore, freshwater animals are relatively
euryhaline, a reflection of the lack of “average” chemistry in lakes, in contrast to the
chemical uniformity
of the marine habitat
(Pennak 1985).
For some taxa, such as echinoderms and
protobranch bivalves, the salinity barrier
appears to be obligate, but most groups
characteristic of one habitat have representatives in the other habitat. Oligochaetes are
a distinctly freshwater and terrestrial group,
yet there are marine tubificids from the intertidal region down to the abyssal plain in
deep-sea benthos. Chironomids, characteristically dominant in lake benthos, have intertidal marine species and can also dominatc the macrobenthos
of saline lakes,
existing in waters with salinities as high as
100% (Timms 1983). Some purely marine
chironomid genera have secondarily reinvaded freshwater habitats (Remane and
Schlieper 197 1). There are no known unionid bivalves in the marine realm; requirements of their glochidea larvae for specific
fish hosts may restrict them to freshwater
habitats. Sphaeriacean bivalves have in-
Lopez
948
Table 1. Comparison of trophic/functional
groups in marine and freshwater muds. (Choice of functional
groups based on Parsons et al. 1984; Jumars and Fauchald 1977; Cummins and Klug 1979.)
Representative
Trophic/functional
group
-
marine
taxa in
-
--
freshwater
Suspension feeders
Mobile infaunal
Sessilc infaunal
Mobile epifaunal
Sessile cpifaunal
“Interstitial”
Mercenaria
Sabellarids
Argopecten
Crassostrea
??
Corbicula
Chironomus
Trichopterids
Spongilla
Pisidium
Deposit feeders
Surface mobile infaunal
Surface scssile infaunal
Surface mobile epifaunal
Subsurface mobile infaunal
Subsurface conveyor belt
Browsers/shredders
Epifaunal predators
Infaunal predators
Nonparticle feeders (DOM or sulfide)
Tellinids
Terebellids
H olothurians
Protobranchs
Maldanids
Sea urchins
Busycon
Nemcrteans
Pogonophorans
Chironomids
??
Amphipods
Naidids
Tubificids
Chironomids
Chaoborus
Leeches
??
vaded marine intertidal habitats (Morton
1983). Although pisidiids are considered to
be intolerant of brackish conditions (Remane and Schlieper 197 l), a Pisidium species has been found in salt pools in northern
Africa (Beadle 1943).
Several genera of amphipods are well represented in both fresh- and marine waters.
Pontoporeia qfinis, a glacial freshwater relict that probably evolved from landlocked
populations of the marine species Pontoporeia femorata, has now reinvaded the
brackish Baltic.
The converse occurrence of typically marine groups in freshwater is well established;
this is particularly true for marine relicts in
the Pontocaspian
region (Remane and
Schlieper 197 1). Polychaetes are represented in freshwater by nereids (Nereis limnicola), ampharetids (Hypania spp.), sabellids (Manyunkia
spp.), and spionids
(Boccardia spp.) (Remane and Schlieper
197 1; Blake and Woodwick 1976). Several
bivalve families (e.g. mytilids, solenaceans,
and arcs) also have freshwater representatives.
Trophic/functional groups- Benthic animals can also be classified into functional
groups in terms of food source, mode of
feeding, and position in the sediment (Jumars and Fauchald 1977; Parsons et al.
1984). Woodin (1983) discussed grouping
marine animals by their effect on the physical stability of the sediment. In their review
of stream invertebrates, Cummins and Klug
(1979) categorized animals as shredders,
collectors, scrapers, piercers, and predators.
Table 1 contains a composite list of important functional groups in sediments. There
are representatives of most trophic/functional group categories in both freshwater
and marine muds, although there is little
taxonomic similarity; different taxonomic
groups are doing rather similar things in the
sediment.
The importance of tentacles- Marine and
freshwater muds are both dominated by deposit feeders. In marine benthos, tentaculate deposit feeding may be the single most
imlportant mechanism for both surface and
subsurface deposit feeding, including many
polychaete families, protobranch bivalves,
and many holothurians. Particle collecting
by tentacles is widespread and may have
important consequences for particle selection (e.g. Jumars et al. 1982). Tentaculate
feeding may be inherently more selective
than other deposit-feeding
mechanisms
(Whitlatch 1980).
In contrast, tentaculate deposit feeders are
essentially absent in freshwater muds, except for occasional polychaetes such as
Benthic macrofauna
Manyunkia and Boccardia (Blake and
Woodwick 1976). Why are tentaculate animals so rare in lacustrine environments?
One possibility is that groups capable of
making tentacles are restricted to marine
environments.
Such taxonomic restriction
infers that only certain phyletic groups are
capable of evolving tentacles, and those
groups have not penetrated freshwater. This
is the likely explanation for protobranchs
and echinoderms, which are restricted to the
marine realm. A few tentaculate polychaetes have invaded freshwater, indicating
that tentacles are not necessarily incompatible with life there. A tentacle is simply an
elongated, flexible, and movable process of
tissue, usually ciliated and having mucus
cells. At the risk of tautological reasoning,
it is worth asking why no freshwater groups,
such as oligochaetes, have evolved tentacles. Tentaculate deposit feeders, at least
nonmobile surface feeders, need steady advection of new particles, which is well provided by tidal motion in marine environments (Nowell et al. 1984). Freshwater
tentaculate polychaetes, such as the sabellid
Manyunkia, appear to be common mostly
in rivers (Remane and Schlieper 1971). If
there are freshwater animals that have
evolved tentacles for deposit feeding, they
might be expected in old river systems like
the Amazon or the Mekong, where particle
advection has been an evolutionary factor.
Interstitial suspension feeding- Suspension feeders on phytoplankton
and suspended organic detritus are well represented
in both marine and lacustrine environments. Bivalves dominate this tropic/functional group, and freshwater and marine
species are morphologically
very similar
with respect to particle-collecting
mechanisms. There is evidence that interstital suspension feeding, that is, collecting and feeding on particle suspended in the interstitial
water, is well represented only in freshwater
habitats. Radiotracer experiments with natural interstitial bacteria showed that Pisidiurn casertanum and Pisidium conventus, two
small pisidiid bivalves dwelling in soft muds
of lakes, filter, ingest, and absorb interstitial
bacteria (Lopez and Holopainen 1987). Microscopic counts indicated that bacterial
abundance in the pore water of lake muds
949
is as high as lo9 cells ml-‘, while preliminary counts in marine muds have been lo2
lower (Lopez and Holopainen
1987;
McDaniel
unpubl.). Whether interstitial
bacterial abundance is typically higher in
lake muds (total bacterial counts are similar) is unknown. The marine corbiculid
Polymesoda erosa, which is found in intertidal mangrove muds, filters particles from
“subterranean”
water, especially from crab
burrows at low tide (Morton 1976). Tnterstitial suspension feeding may be important
only for small animals supplied with a concentrated food source (Lopez and Holopainen 1987; Mallatt 1982). There may be marine animals that are interstitial suspension
feeders, but it is doubtful that they are as
important as Pisidium spp. are in lake muds.
Food sources
Major categories of food-Potential
food
sources for nonpredatory animals in both
lacustrine and marine muds include phytoplankton, benthic algae, vascular plant litter, particle-associated microorganisms, especially bacteria and fungi, a wide range of
detrital organics, and dissolved organic
matter. Some coastal marine environments
are dominated by the input of seaweeds and
streams and smaller lakes by leaf fall of vascular plants. Organic deposition in larger
lakes and in marine areas not dominated by
proximate seaweed or marsh areas is characterized by sedimenting phytoplankton
or
phytodetritus,
including zooplankton fecal
pellets.
For most deposit-feeding animals dominant in muds, both microbial and detrital
foods appear necessary for meeting nutritional demands (Lopez and Levinton 1987).
Extracellular
polymers released by sedimentary microbes may be an important link
between microbial and detrital pools (Baird
and Thistle 1986). Deposit feeders appear
to be very capable of digesting sedimentary
microbes (Fenchel 1970; Hargrave 1970;
Kofoed 1975; Baker and Bradnam 1976;
Cammen 1980a; Harper et al. 198 l), and
many may be limited by microbial abundance (Bianchi and Levinton 1984; Ward
and Cummins 1979; Barlocher and Kendrick 1973). Except for surface sediments
in very shallow water, which harbor high
950
Lopez
densities of benthic microalgae, microbial
abundance in sediments appears to be far
too low to meet energy demands, given
measured ingestion rates and organic absorption efficiencies (Baker and Bradnam
1976; Moore 1979; Cammen 1980a; Bowen
1980; Butler 1982; Findlay and Meyer
1984). Bacteria typically account for < 1%
of the organic carbon in sediments (i.e. Rublee 1982) yet absorption of ingested sedimcntary organic matter by deposit feeders
is usually in the range of 2-20% (Brinkhurst
and Austin 1979; Cammen 1980b; Johannsson 1980; Johnson 1985). Fungal carbon does not meet carbon demands of the
freshwater isopod Lirceus sp.; fungi appear
to be more important as modifiers of leaf
substrate than as a food source (Findlay et
al. 1986; Barlocher et al. 1978). In general,
there appears to be no systematic difference
between marine and lacustrine animals in
the range of absorption efficiencies of scdimentary microbes or detritus.
There is evidence that digestion of partially humilied organic matter is better developed in certain freshwater insect larvae
than in any group of marine animals. The
alkaline midgut (pH > 11) of the stream
diptcran Tipula abdominalis serves to dissociate the tannin-protein
complexes of decomposing organics (Martin et al. 1980).
This is undoubtedly important for a nitrogen-limited animal, as perhaps, for many
deposit and detritus feeders (Tenore and
Rice 1980). Alkaline digestion should make
available certain protenoids associated with
humified organic matter (Rice 1982). A
similar strategy is well developed among
phytophagous lepidopteran larvae- species
feeding on high-tannin plants having higher
midgut pH (Berenbaum 1980). A highly alkaline midgut (> 10) is also characteristic of
mosquito larvae that feed on organic detritus and microbes (Dadd 197 5). Based on
studies of freshwater animals, Lamberti and
Moore (1984) suggested that the midgut pH
of invertebrate consumers was, in general,
either neutral or alkaline and that these nonacidic conditions promote the dissociation
of ingested protein, such as in protein-tannin complexes.
This dots not seem to be the case for
marine invertebrates. Typical values of pH
optima of digestive enzymes in marine invertebrates range from 5.5 to 8.5 (Reid and
Rauchert 1972; Michel and Devilliz 1978).
I am not aware of highly alkaline values in
marine detritivores. This difference might
be Idue to the local importance of vascular
plant debris in freshwaters. If the primary
value of alkaline proteases is digestion of
humic- or tannin-bound protein, their presence might bc expected in animals that ingest deeply buried, anoxic sediment.
The role of dissolved organic matter-One
of the most intriguing differences between
marine and freshwater benthic fauna is in
the ability to take up and use dissolved organic matter (DOM). Virtually all soft-bodied marine invertebrates exhibit excellent
active transport mechanisms for transepidcrmal uptake of small molecules such as
amino acids (Stephens 1982). It has been
demonstrated that molecules are taken up
actively and used metabolically,
but their
nutritional or metabolic importance has yet
to be elucidated. The idea that “normal”
marine invertebrates possessing typical alimentary ‘tracts require DOM to meet respiratory demands has been subjected to repeated debate (first between Putter and
Kr’ogh, see Jorgensen 1976), and there have
been several recent reviews (i.e. Jorgensen
19’76; Sepers 1977; Siebcrs 1982; Stephens
1982).
In contrast to marine animals, freshwater
invertebrates exhibit very poor uptake abilities (e.g. Efford and Tsumura 1973). Sepers
(1977) noted that it is remarkable that uptake in freshwater invertebrates proceeds at
a much lower rate or is completely absent.
A comparison between Nereis succinea and
Nereis limnicola demonstrated that the uptake rate greatly declined when salinity was
reduced to 13?&- the salinity at which osmoregulation
begins (Stewart 1979). Osmoregulation and DOM uptake may be mutually incompatible (Stephens 1967); many
of the specific uptake mechanisms are Na-’
dependent and the ionic and osmotic nature
of freshwater may constrain DOM uptake
by soft-bodied invertebrates.
If DOM uptake does in fact meet a high
percentage of the respiratory demands of
marine animals (Stephens 1975) then one
would expect secondary production of ma-
Benthic macrofauna
rine benthos to be higher for a given organic
input to the bottom. Although a rigorous
comparison is difficult, there does not appear to bc a systematic difference in secondary production between marine and lacustrine benthos. This would be consistent
with Siebers’ (1982) suggestion that epiderma1 transport of small organic molecules
plays a minor role as a source of energy in
aquatic organisms, but that it rather reflects
a general property of the membrane cella conclusion that is also consistent with the
vestigial nature of the transport systemsand that the real benefit of the uptake mechanisms may be to prevent loss of the pool
‘of body amino acids.
One of the few examples of substantial
uptake ofdissolved organics in lower salinity water was demonstrated for the nematode Adoncholaimus thalassophygas, which
was able to take up dissolved glucose from
brackish water (5%) (Lopez et al. 1979).
Unlike uptake by marine organisms, uptake
by oncholaimids is not transepidermal, but
occurs via the intestinal wall (Chia and Warwick 1969). DOM may be collected by adsorption as pharyngeal mucus, and the mucus bolus is then swallowed (Riemann and
Schrage 1978). This mechanism of DOM
uptake may proceed simultaneously
with
osmoregulation, but its existence in freshwater animals has not been studied.
A recent study demonstrated that the
Tubifex tubifex
freshwater
oligochaete
takes up acetate and propionate as well as
marine invertebrates (Hipp et al. 1986). The
uptake mechanisms are Na+-dependent.
Chemoautotropy
in marine animals-
Most marine animals that exhibit substantial uptake of dissolved substrates have typical alimentary morphologies, but there are
several examples of free-living marine animals that are mouthless and gutless, including all pogonophorans, some bivalves
(Reid and Bernard 1980; Fisher and Hand
1984) and even a tubificid
oligochaete
(Giere 198 1). To my knowledge, there have
been no descriptions of free-living freshwater animals lacking a typical digestive
tract. Endosymbiotic, sulfide-oxidizing
bacteria appear to provide the primary energy
source for these animals (Felbeck 1983;
Cavanaugh 1983; Felbeck et al. 1983). Be-
951
cause of the high sulfate concentration of
seawater, there is significant bacterial sulfate reduction in marine sediments, resulting in a high sulfide flux. Sulfide flux due to
putrefaction can be high in freshwater muds,
but it is not a characteristic feature of lacustrine waters (Laanbroek and Veldcamp
1982; Capone and Kiene 1988). The evolution of this particular endosymbiosis is
apparently favored only in marine waters.
Gut symbionts are certainly present in
freshwater animals. Cummins and Klug
(1979) observed bacteria attached in the
hindguts of many stream invertebrates, especially in animals ingesting the most refractory diets. Given that lake sediments are
characterized by methane rather than by
sulfide flux (Capone and Kiene 1988) it is
interesting to speculate that methane-oxidizing bacteria are more likely to be found
as endosymbionts in freshwater animals.
Physiological adaptations
Osmotic regulation -The
most obvious
physiological difference between marine and
freshwater fauna is the presence of efficient
mechanisms for osmotic control and adjustment characteristic of freshwater animals; they are remarkably euryhaline over
a wide range of low salinity (Pennak 1985).
The hypotonic nature of freshwater relative
to body fluids makes such osmotic regulation a necessity. Pennak (1985) suggested
that this osmotic work results in higher oxygen demand, since freshwater invertebrates
use more oxygen than do their marine counterparts.
Anaerobiosis - The water overlying organic-rich muds is susceptible to oxygen depletion, particularly during periods when a
stratified water column reduces mixing. This
problem is compounded in summer with
enhanced microbial respiration. Therefore,
many poorly mixed bodies of water experience sustained periods of hypoxia or anoxia. This is particularly the case in all but
very shallow lakes, due to the lack of tidal
mixing.
Many invertebrate species in freshwater
and marine sediments can live for a few
hours to a few months without oxygen, but
freshwater animals have more frequently
developed the physiological
mechanisms
952
Lopez
needed to withstand anaerobic conditions
for long periods than is the case for marine
animals (Pennak 1985). In Lake Tiberias
(Sea of Galilee), the hypolimnion
is anoxic
for 8 months of the year, but the sediments
are inhabited throughout by several species,
including the tubificid oligochaete Euilyodrilus heuscheri (Por and Masry 1968). It
reproduces at peak anoxia, and animals
maintained in anoxic bottles were “visibly
active” .for 4 months. Similarly, Lindemann
(1942) kept tubificids for > 120 d under anoxia. Another oligochaete, Tubijkx tub@x,
can survive, reproduce, and grow under
continuous
anoxia lasting
10 months
(Famme and Knudsen 1985).
In Lake Esrom, Chironomus anthracinus
stops growing during summer stagnation,
but starts again immediately after the overturn (Jonasson 1972). Hemoglobin certainly helps chironomids and other animals to
survive such conditions (perhaps with the
subsequent evolution
of impalatability:
Hutchinson
198 1). It is remarkable that
much of the benthos survives these prolonged anoxic periods, which are rather unpredictable in duration and frequency.
In contrast, marine benthic animals (particularly in the intertidal)
appear to be
adapted to relatively short periods of anoxia, but they do not survive prolonged anoxic stress. Summer stagnation does occur
in estuaries and coastal regions and may
cause catastrophic mortality of the macrofauna. However, during subsequent aerobic
periods, the benthos is rapidly colonized by
typical postdisturbance
species (Officer et
al. 1984).
The opportunistic clam Mulinia lateralis
is unusual in maintaining high feeding and
locomotor rates under anoxia (Shumway et
al. 1983). It maintains the same rate of meta bolic heat dissipation under anoxic and oxic
conditions, which reflects its adaptation to
short-term instead of chronic oxygen deficiency and may explain its brief anoxic survival times (< 10 d).
Some marine meiofauna, such as the
Gnathostomulida
and some turbellarian
familes, are almost completely restricted to
reduced sediments (Powell et al. 1979).
These animals may not be obligate anaerobes; many of them may be microaero-
philic, and they exhibit adaptations
with long-term exposure to H2S.
to deal
Animal biomass and secondary
production
Macrofaunal
production
of lakes and
oceans is compared here both in terms of
community production (total production of
all component species) and production to
biomass ratios (P : B) of individual
species.
The biomass of macrofauna is controlled
by the amount of organic matter deposited
each year and is a function of primary production and depth. In shallower reaches,
benthic primary production can be the most
important carbon source for the benthos
(Strayer and Likens 1986). Deep lakes never
have high benthic biomass, while shallow
lakes have a wide range of values (Deevey
1941). Similarly, the high temperatures of
tropical lakes reduce the amount of detritus
that reaches the bottom and the ratio of
benthic to primary production compared to
temperate lakes (Morgan et al. 1980). There
is a general logarithmic decrease of animal
biomass with depth in the ocean (Rowe
19’71). In coastal sediments, macrofaunal
biomass generally falls within l-l 6 g dry wt
m-‘2 (Mann 1982). Faunal biomass in lake
sediments is in the same range. Deep, oligotrophic lakes may be as low as 0.1, and
temperate, shallow lakes may support a biomass of 15 g m-2 (Morgan et al. 1980;
Wetzel 1983; Likens 1985). Very old lakes
aplpear to have higher profundal biomass at
a given depth, compared to young lakes;
Lake Ohrid has 10 g me2 at 200-m depth,
and Baikal has 0.5 g me2 at 500 m (Morgan
et al. 1980). Thus, there is a basic similarity
in the relation of primary production and
depth to secondary macrofaunal production
in lakes and seas. Mann (1980) noted that
from an input of 2,000 kcal m-2 yr-l (200
g), benthic secondary production in shelf,
rivers, and lakes is generally between 200
and 400 kcal. For most shelf and lacustrine
environments,
secondary benthic production falls within the range of l-10 g dry wt
m-2 yr-’ .
In St. Georges Bay, the Gulf of St. Lawrence, the lowest rates of organic supply to
the benthos occurred during summer strat-
Benthic macrofauna
ification (Hargrave and Phillips 1986). During this period, organic sedimentation
to
22-m depth amounted to 20% of the primary production, although about 60% sedimented when the water column was mixed.
The estimated macrobenthic production at
22 m in St. Georges Bay changed from 20
to 45% of the particulate organic carbon
sedimentation for stratified and unstratified
periods, although production may have been
overestimated by use of a P: B ratio of 2.
Decomposition
of the sedimented organics
was very rapid.
Although the focus of this review is on
macrofauna, it is worth commenting on the
importance of meiofauna in secondary bcnthic production.
Nematodes and microcrustaceans dominate both marine and
freshwater
meiofauna.
In marine sediments, meiofaunal biomass is 10-l to lO-2
that of macrofauna, but because of high
weight-specific metabolism, the meiofauna
can account for a substantial fraction of benthic secondary production (Gerlach 197 1).
There is much less information
on meiofaunal species in lakes where their role has
received relatively little attention (Strayer
and Likens 1986). In Mirror Lake, meiobenthos accounts for approximately 30% of
macrobenthic biomass (Likens 1985).
The relative importance of meiofauna
may be highest in brackish water, where
there has been minimum success by either
freshwater or marine macrofaunal species
(Gerlach 1971; Elmgren 1984). The meiobenthos also accounts for a high proportion
of biomass under food-poor conditions,
such as in oligotrophic lakes (Morgan et al.
1980) and in deep-sea sediments (Thiel
1975).
The standing stock of benthic animals
often appears insufficient to meet the metabolic demands of predators. This apparent
problem, sometimes called the Allen paradox, lays proper stress on the importance
of the turnover of benthic biomass. Calculation of production to biomass ratios (P:
B), which is sometimes referred to as turnover ratio (TR), allows comparison of production of populations differing in biomass.
Based on studies of freshwater animals,
Waters (1969) suggested that, within the
lifespan of a cohort, the P: B ratio is 2.5-
953
6, with a modal value of 3.5. This agrees
well with the average value in a comparison
of studies on 55 marine benthic species
(Parsons et al. 1984).
Because cohort P : B normally falls within
a relatively narrow range, annual P : B is
mainly a function of generation time. Species
having a very short generation time will obviously have higher annual P : B values.
There is a general inverse relationship between body size and generation time; small
animals tend to have higher P : B values
(Banse and Mosher 1980). Annual P: B is
sensitive to environmental
factors controlling generation time, including food input
and temperature (Johnson and Brinkhurst
197 1). The quality of the diet is also an
important factor. Morgan et al. (1980) noted
that, for freshwater animals, the long generation times of species feeding below the
mud surface (Tubificidae, Pisidium) compared with surface feeders (Chironomidae)
may result from the different quality of food.
The same trend is clear for marine species.
Basic life history parameters and environmcnts factors thus control annual P : B, and
there is no characteristic difference between
marine and freshwater species.
Measurement of annual P : B is dependent on clear identification
of cohorts. In
lacustrine environments,
chironomids
are
relatively well studied, partly because they
are often the dominant group, but also because discrete cohorts are usually easy to
define (Benke 1984). In contrast, there are
fewer P: B estimates for tubificids because
their reproduction
and growth make cohorts difficult to identify (Wetzel 1983). In
a study of the tubificid Potamothrix hammoniensis, Jonasson and Thorhauge (1976a)
were able to separate four year-classes and
thus could estimate annual population production. Annual P : B values ranged from
0.58 to 1.35. Jonasson and Thorhauge
(1976a) suggested that low turnover may be
common for tubificids in the profundal area
of stratified lakes, where low water temperatures and perhaps anoxic conditions prevail for long periods. Hargrave and Phillips
(1986) suggested that similarities
in production estimates result from applying
equivalent annual turnover ratios to similar
values of biomass. For example, macro-
954
Lopez
benthic organisms in Long Island Sound and
St. Georges Bay have a similar standing crop
(m 10 g C m-2) and similar annual turnover
ratios [2.4 derived from the calculated production rates of Sanders (1956) and 2 assumed in the study of Hargraves and Phillips (1986)].
Population dynamics and
community structure
Reproduction and dispersal-The
general
rule among marine benthic macroinvertebrates is a life history of sexual reproduction
resulting in larvae that may be dispersed
considerable distances before settlement and
metamorphosis.
Sexes are generally separate. Timing of reproduction
usually correlates with seasonal changes in temperature and with lunar cycles, and success of
the next generation frequently depends on
the availability of food for planktonic larvae
(Barnes 19 56). In temperature waters, about
70% of the benthic invertebrates
have
planktonic
(planktotrophic
or lecithotrophic) larvae (Thorson 1950). Larvae of some
species are able to survive in the plankton
for long periods (> 100 d) and can be dispersed across ocean basins (Scheltema 197 1).
lf a larva survives the hazards of planktonic
life, it must prepare for metamorphosis and
choose a proper substrate for settlement.
Predation and competition
are probably
significant problems for newly settled juveniles. Considerable literature exists concerning the hazards and rewards of having
planktonic larvae, the effects of dispersal on
gene flow, larval settlement, and mortality
of recently settled animals (e.g. Strathmann
1980; Jablonski and Lutz 1983). Even
though some animals may spend months in
the plankton, the larval period is typically
a small fraction of the lifespan of the animal,
so most of their life is spent in the benthos.
Asexual reproduction appears to be more
important for freshwater benthic animals,
primarily due to the importance of oligochaetes. As in many freshwater zooplankton, sexual reproduction is timed to declining habitat quality and is often used to
produce resting stages (Pennak 1985).
The chironomids, the most important insect group in freshwater muds, spend most
of their life as benthic larvae. The larval
period of a few weeks to 2 yr is followed by
a short, nonfeeding, breeding and dispersal
adult stage. Reproduction is sexual.
Planktonic larvae are rare in freshwater
environments. In Lake Baikal, the sabellid
polychaete Manyunkia baikalensis does not
form a free-swimming trochophore, unlike
its marine congeners (Kohzov 1963). The
mytilid bivalve Dreissena poiymorpha, a recent invad.er of freshwaters, however, does
produce planktonic larvae. In contrast, the
marine gastropods Melampus bidentatus and
Amphibola crenata are unusual among pulmonates in having planktonic larvae.
Freshwater invertebrates appear to produce fewer, larger eggs that are held until
hatching and release of young (Pcnnak
1985). This may related to the need for
young animals to hatch with fully developed
osrnoregulatory capabilities.
Lakes are discrete and relatively ephemeral features of the landscape, yet even rcmote lakes are rapidly colonized by benthic
animals. Flight by winged adults results in
considerable dispersal of insects, but for
noninsect species, resistant eggs and cysts
appear to be important for overland transpo:rt. Pennak ( 1985) noted that this ease of
colonization
greatly surpasses any such
mechanisms among their marine relatives.
The small size of many freshwater benthic
species allows aerial dispersal by wind, or
more likely, by winged organisms. Fryer
(noted by Davis 1982) found that 20% of
the corixids examined had at least one Pisidium clamped to a leg. The unionid bivalves exhibit an exotic means of dispersal,
having larvae that are parasitic on fish.
Initial distribution of larval chironomids
is controlled by egg-laying behavior; most
species oviposition near the shoreline (Davies 1976). Accumulations
of floating eggs
along wind-exposed reaches can result in
very high densities of newly hatched larvae.
The first instar of many species of chironomids is planktonic, having morphological
and behavioral characteristics that differ
from the more sedentary later instars. This
planktonic period results in secondary dispersal and redistribution
of larvae within a
basin. Similar movement of marine postlarval animals is also widely documented
(Dewitt 1985).
Benthic macrofauna
Biotic eflects on community structureCompetition and predation are fundamental in controlling benthic community structure, although the nature of the sedimentary
environment
has made it very difficult to
conduct manipulative experiments. Woodin (1983) noted that indirect interactions
involving
density-dependent
modification
of the substrate or pre-emption of resources
are well known, important phenomena in
infaunal systems (see also Woodin and
Jackson 1979).
The effects of resident infauna on colonizing larvae have been well documented in
interacmarine sediments; “adult-larval”
tions can be the result of ingestion or burial
of the larvae by the adults (Woodin 1976).
A recent experimental study (Elmgren et al.
19 8 6) corroborated Segarstrale’s ( 1962) theory that dense populations of the depositfeeding amphipods P. afinis and P. femorata increase mortality of postlarval Macoma balthica by incidental predation, and
thereby control its distribution in the Baltic
Sea. High mortality of juveniles may depress community
biomass below carrying
capacity, as suggested by Peterson (1979),
but this does not seem to be the case in the
Baltic (see also Evans 1983). Elmgren et al.
(1986) pointed out that where such interference is strong, species with brood protection likely become dominant, as are Pontoporeia spp. over large areas of the Baltic
Sea.
Similar processes have been described for
lake muds, but with an interesting twist. The
profundal zone of Lake Esrom, Denmark,
is dominated by C. anthracinus (Jonasson
1972). It takes 2 yr for this species to mature
in this zone. During spring, it suspension
feeds on phytoplankton, but during summer
stagnation, surface deposit feeding becomes
important, and larval density is so high that
the entire mud surface is scraped and ingested by chironomids. This presumably results in high egg mortality, so there is no
recruitment of another generation. Also, this
nonspecific predation appears to control the
life cycle of the tubificid oligochaete, P.
hammoniensis, probably by ingestion of cocoons and also by competition
for food.
Some chironomids pupate and emerge after
1 yr, especially in shallower water, but in
955
the profundal zone, high densities (>2,000
mm2) of larvae remain. In the second year
the remaining larvae pupate and then literally fly away, leaving an empty benthic
habitat behind. Subsequent recruitment of
chironomids and oligochaetes is very strong.
Thus there is a 2-yr cycle in abundance of
benthic organisms in the profundal zone of
Lake Esrom, which is driven by the growth
rate of the dominant chironomid.
Littoral
populations of P. hammoniensis appear to
be controlled mainly by predation by fish
and invertebrates, while profundal populations are controlled by competition with
C. anthracinus (Jonasson and Thorhauge
1976b).
Such periodic emptying of the benthos
seems to be a peculiar aspect of lacustrine
systems and is a consequence of the life cycle
of insects having an aquatic larval stage and
a terrestrial adult stage (Hutchinson 198 1).
Marine benthic habitats are similarly emptied only by disturbance. Marine species are
typically benthic as adults, and reproductive propagules are sent off. The adult corpus remains.
Macan (1970) noted the paucity of insect
larvae in sediments affected by sewage pollution, although flatworms, isopods, amphipods, gastropods,
and leeches were
abundant. When sewage enrichment
increases the main food supply, predation
pressure on insects and other animals with
unprotected eggs is high. Flatworms and
leeches enclose their eggs in a tough cocoon,
snails enclose their eggs in a mass of jelly,
and pcricarids carry their eggs. The suggestion is that under productive conditionswhere these carnivorous and detritus-feeding animals abound- certain insects are absent because they are not adapted to meet
the resulting predation.
Predation by leeches can be the main
source of mortality to chironomid populations; the reduced density that results produces increased chironomid
growth (Rasmussen 198 5). Thus growth rate and number
of seasonal generations are partly determined by density effects. A similar process
has been suggested for a tubificid (Jonasson
and Thorhauge 1976b).
Peterson ( 1979) concluded that predation
lowers biomass and diversity of marine sed-
956
Lopez
imentary fauna. Similar effects on freshwater benthic communities have been observed after the addition of predatory fish
to lakes (Post and Cucin 1984).
Exploitative
and interference competition appears to have a major effect on growth
and survival of benthic animals. The growth
of younger instars of Chironomus plumosus
is lowered both by high densities of older
instars and by periodic stirring of the mud,
suggesting that mechanical disturbance of
tube-building activity can limit growth (Kajak and Warda 1968). In marine muds, the
burrowing activity of the highly mobile bivalve Yoldia limatula disturbs the burrowbuilding activity of Solemya veium (Levinton 1977).
The importance of competition for food
is a function of the seasonal food input and
the functional/trophic
groups involved. In
a eutrophic pond, the deposit-feeding C. anthracinus exhibited lower seasonal variation in carbon and nitrogen absorption than
did the suspension-feeding
C. plumosus;
there was lower absorption during summer
when the plankton was dominated by flagellates (Johnson 198 5). Surface depositfeeding Chironomus riperius grew rapidly
after experimental addition of freshly sedimented microdetritus,
but suspensionfeeding Glyptotendipes paripes showed no
response (Rasmussen 1985). There were
strong intraspecific density effects that reduced growth rates for both species, but there
were only weak interspecific effects between
the suspension feeder and the deposit feeder. Strong density effects within the suspension-feeding chironomid were similar to
effects of density manipulations
of marine
suspension-feeding
bivalves
(Peterson
1977).
Macoma balthica, a marine bivalve capable of both suspension and deposit feeding, exhibits density-dependent growth when
deposit feeding, but not when suspension
feeding (Olafsson 1986). In a study of the
Lake Esrom benthos, C. anthracinus grew
to full size and emerged when it was fed
enriched surface sediments, but starved
when fed subsurface sediment; the subsurface deposit-feeding
oligochaete Potamothrix sp. could grow on the deeper sediment
(Jonasson 197 8).
In Narragansett Bay, the late springtime
increase in the deposit-feeding benthos appeared to be in response to warmer temperatures which allowed the benthos to feed
on the deposition of the early-spring diatom
bloom (Rudnick
et al. 1985). Lowered
growth and survival in the summer occurred when respiratory demands exceeded
fresh organic input to the benthos (Grassle
et ,al. 1985).
Succession-Community
succession is an
important topic in both marine and freshwater benthic research, and this review will
provide evidence of functional similarity.
Benthic colonization
and subsequent processes in lakes have frequently been examined in terms of island biogeography,
which is well suited for discrete habitats
(Barnes 1983). Because of the open, continuous nature of the marine realm, there has
been greater emphasis on processes following some physical disturbance. Classic work
on the succession of vegetation (e.g. fire climax) provides a more relevant context for
such study. Connell and Slatyer (1977) distinguis hed between facilitation,
tolerance,
and inhibition
as possible successional
mechanisms, but pointed out that direct
evidence on mechanisms is available only
for the earliest stages, during which many
species are short-lived and amenable to experimentation.
IBenthic succession in marine sediments
after disturbances such as storms, oil spills,
organic pollution, or periodic anoxia may
be controlled by geochemical conditioning
of the sediment by bioturbating
animals
(Pearson and Rosenberg 1978; Rhoads and
Boyer 1982; Larson and Rhoads 1983). Following a physical disturbance which removes the ambient fauna or creates a new
habitat, species that arrive early are typically tolerant of the harsh geochemical conditions of anoxic mud; Capitella larvae even
use sulfide diffusing from the sediment as a
settlement cue (Cuomo 1985). Typically, the
ea:rly colonizers are small, rapidly growing
tube-dwellers, feeding either on surface sediment or on suspended seston. Important
groups include capitellid and spionid poly:
chaetes and ampeliscid amphipods. Feeding
and respiratory currents of these small animals serve to oxidize the surface layer of
957
Benthic macrofauna
sediment. Later successional stages are
characterized by larger, deeper dwelling animals that feed on deeper layers of sediment.
Representative
animals during this later
successional stage include maldanid polychaetes and protobranch bivalves. These
animals may require that the sediment is
conditioned to maintain proper microbial
activities.
Similar processes seem to occur in the
colonization of lakes (Table 2). This process
has typically been studied by following the
colonization of a new habitat, such as a reservoir. Chironomid larvae are typically the
first colonizers of new benthic habitats
(Cantrell and McLachlan 1977; Street and
Titmus 1979). This must be due in part to
the great dispersal abilities and high fecundity of the winged adults, but they are functionally equivalent to the early marine colonizers: relatively small, tubicolous, surface
deposit feeders or suspension feeders with
the capacity for rapid growth. The genus
Chironomus appears especially tolerant of
anoxic conditions typical of newly flooded
reservoirs (Street and Titmus 1979). In new
habitats that are not organically enriched,
the genus Tanytarsus is also an important
colonizer (Cantrell and McLachlan
19 7 7).
The amphipod Hyalella azteca, another
small tube-dweller, is also a common early
colonist in new or disturbed habitats (Voshell and Simmons 1984; Fuller and Cowell
1985).
Naidid oligochaetes are also typically early colonists; they are also found primarily
in the near-surface layer of sediment (Pfannekuche 198 1.) In contrast, tubificids are
almost always deeper dwelling, head-down
feeders and exhibit more stable populations
over time. In a comparison of ponds ranging
in age from 0.5 to 15 yr, Barnes (1983)
showed that naidids accounted for 100% of
the oligochaetes in lakes younger than 3 yr,
and tubificids made up 70% of the worms
in older lakes. In one study of benthic development in a reservoir, the “most striking
change” in the second year was the “sudden
appearance of large numbers of oligochaetes,” suggesting that conditioning
of
sediment organic quality is important for
oligochaetes (Voshell and Simmons 1984).
Therefore, the temporal succession of func-
Table 2. Comparison of successional groups in marine and freshwater muds. (Successional sequence of
benthic macrofauna based on Rhoads et al. 1978.
Freshwater examples taken from various sources.)
Marine
Freshwater
Early stages
Small surface deposit or
suspension feeders,
high growth rate
Streblospio
Chironomus
Mature stages
Subsurface deposit
feeders, longer lived
Yoldia
Tubificids
Successional
stalus (functional
traits)
tional groups in both marine and freshwater
muds seems to be driven by the effects of
bioturbating
animals on the geochemical
properties of the sediment, even though the
specific taxonomic groups and mechanisms
of colonization differ substantially.
There is a venerable tradition in limnology to use the presence of particular benthic
animals, especially chironomids,
to categorize the trophic conditions of lakes (see
Brinkhurst
1974). This approach has also
been used to investigate the responses of
freshwater benthos to environmental
pollution. Organic pollution results in the presence of species characteristic of eutrophic
lakes; many of these species, like C. anthracinus, are relatively large, sessile tubedwellers that feed by filtration or browsing
around the tube. They are especially tolerant of anoxia (Wiederholm 1984).
Disturbance that does not organically enrich the benthos, such as enhanced inorganic sedimentation, can have a very different effect. Addition of inorganic sediment
dilutes the organic concentration of the sediment, which is essentially oligotrophication. Chironomids
that inhabit transportable cases appear to be favored under
conditions of high sedimentation,
because
they are able to exploit foods at the sediment-water interface, while more sedentary
tube-dwellers would be covered (Wiederholm 1984). Many oligotrophic chironomid
species are small and free-living. A similar
pattern in body size and motility is evident
in a comparison of polychaetes along a depth
gradient in the Pacific Ocean (Jumars and
Fauchald 19 7 7).
958
Table 3. Characteristic
vironmental variables.
Lopez
differences
between marine and freshwater
Interstitial suspension feeding only in freshwater (?)
High midgut pH of some freshwater detritivores
DOM uptake trivial by freshwater animals
Mouthless animals with sulfide-oxidizing
symbionts only in the sea
Better tolerance to anoxia in freshwater animals
Aerial dispersal and resting stages better developed in lakes
_.
macrofauna,
with suggested causal en-
Salinity (?)
Vascular plant input
Salinity, Na+
High sulfate
Mixing by tidal currents
Lakes are “islands”
--
Conclusl’ons
Re,ferences
Table 3 summarizes the differences between the fauna inhabiting freshwater and
marine muds and the suggested environmental factors causing these differences. We
can be reasonably certain about some of the
relationships. It is well established that the
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relationships are more speculative, but the
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marine sediments, is a likely prerequisite for
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bc treated with great suspicion. There may
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biogeochemical
control of proper conditioning of sediment.
These conclusions suggest that formal comparison of marine and freshwater benthos
can substantially enhance our understanding of benthic systems.
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