Freshwater Biology (2000) 44, 149±163

Trophic relationships: integrating meiofauna into a

realistic benthic food web
J. M. SCHMID-ARAYA AND P. E. SCHMID
School of Biological Sciences, QMWC, University of London, Mile End Road, London E1 4NS, U.K.

SUMMARY
1. This paper summarises the most important contributions on trophic relationships of
lotic meiofauna. In contrast to marine research, the few quantitative studies of the
freshwater meiobenthos have shown that these invertebrates not only take up particulate/
fine organic matter, but also dissolved organic substances attached to organic particles. In
lotic ecosystems, further estimates of grazing rate and bacterial/algal ingestion rate are
needed, particularly in situ measurements.
2. The effects of macroinvertebrate predators upon meiofauna are still under debate.
Depending on the type of experiments (laboratory vs. field) it seems that macrofauna may
or may not affect meiofauna. Field samples and analyses of gut contents of larval tanypod
chironomids have shown that the impact upon meiofauna was low and larvae were
nonselective predators. Predation amounted to 2.2% of the combined prey density and
prey consumption averaged 1.3 individuals per predator individual per year.
3. Adding taxonomic resolution by including the meiofaunal component within lotic food
webs distinctly increases the number of total species and, as a consequence, changes food
web statistics. Webs that included meiofauna revealed that these metazoans contributed
substantially to the percentage of intermediate species (species with predators and prey).
The resolution of dietary analyses of major consumers of macro- and meiobenthos showed
that many stream invertebrates feed on meiofauna.
Keywords: feeding habits, Meiofauna, stream food webs, trophic relationships

Introduction incorporated into the detrital trophic complex (Tenore

& Rice, 1980), and the data of Escavarage, Garcia &
Meiofauna have received much attention from marine
Castel (1989) incorporated detritus into the energy
biologists but have largely been neglected by fresh-
budget of meiofauna in marine systems.
water ecologists. In the marine environment, meio-
On the other hand, planktonic food webs in lakes
fauna plays an important role as a trophic link
can include taxa and size ranges equivalent to that of
between bacteria and larger fauna, enhancing the
the stream meiofauna. Such studies have shown that,
rate of: (a) carbon mineralisation by stimulating
in ultraoligotrophic and eutrophic monomictic lakes
microbial activity through predation; and/or (b)
dominated by algal and bacterial picoplankton,
consumption of detritus by larger deposit-feeding
respectively, the cladoceran Daphnia is the keystone
invertebrates (Tenore et al., 1977; Findlay & Tenore,
species facilitating the link between microbial produc-
1982; De Morais & Bodiu, 1984). The close links
tion and higher trophic levels (Porter et al., 1988;
between detritus (either as fine or coarse particulate
Stockner & Porter, 1988). Daphnia can transform both
organic matter), bacteria and meiofauna have been
algal and bacterial picoplankton into suitable size
ranges for consumers such as copepods, cladocerans
like Leptodora, insect larvae such as chironomids, and
Correspondence: J. M. Schmid-Araya, School of Biological
fish. In other monomictic lakes where Daphnia is
Sciences, QMWC, University of London, Mile End Road,
London E1 4NS, U.K. E-mail: [email protected] virtually absent, however, bacterial production is then

ã 2000 Blackwell Science Ltd. 149

150 J. M. Schmid-Araya and P. E. Schmid
related to variations in abundance and production of Interactions within the microbial web can be
macro-zooplankton (crustaceans) and microzooplank- viewed as a transfer of energy and matter to higher
ton (rotifers and ciliates) throughout the year (Pace & trophic levels. However, Arndt (1993) based on
Orcutt, 1981; Orcutt & Pace, 1984). Lampert's assessment (1978), proposed that if
In sediments, microbial production is directly energy-rich compounds are reduced to lower ener-
available to larger consumers (Meyer, 1994). If much getic levels by biological and biochemical degrading
of the benthic microbial community is attached to processes, then small metazoans have a very signifi-
particles, it would be mechanically simpler for a large cant effect on the microbial web via sloppy feeding
(1±10 mm) consumer to ingest a particle of dimension and excretion. Marine nematodes have shown that
10±1000 mm than capturing a free bacterial cell less their excretion products serve as a substrate for
than 1 mm long (Lodge et al., 1988). In addition, the bacterial populations (Rieman & Schrage, 1978).
concentration of interstitial bacteria may be higher In contrast to other aquatic habitats, the main
than in open water. There are few estimates of energy source for lotic systems, particularly low
attached vs. nonattached bacterial populations but order streams, is allochthonous organic matter
data from a limestone stream confirmed that inter- (mainly leaf-litter). This input consequently promotes
stitial water contained at least 102 times higher a microbial-based production and direct and indirect
bacterial density than free water and 90% of the bacterial consumption may extend over several
bacteria were attached to particles (Kasimir, 1990). trophic levels, and bacterial production must support
In lotic ecosystems, some debate has developed over the microfauna (i.e. flagellates, protozoans It is now
whether or not meiofauna influence bacterial produc- becoming clear that the meiofauna contributes to the
tion (Hakenkamp & Morin, 2000). Perlmutter & Meyer biodiversity of stream/rivers in terms of species
(1991) demonstrated that some harpacticoid species richness (Robertson, Rundle & Schmid-Araya, 2000)
were able to consume bacterial-C one to four orders of and by a variety of trophic processes: consuming
magnitude greater than leaf-shredding macroinverte- bacteria and algae and prey, by being eaten and by
brates. Borchardt & Bott (1995) found that meiofauna recycling nutrients.
ingest only a small fraction of the bacterial production, The objectives of this paper are to: (a) summarise
except when rotifers and large ciliates were abundant. recent findings about meiofaunal feeding; (b) indicate
Their results also showed a high grazing pressure on those taxa that depend on meiofauna as food in lotic
diatoms by some meiofauna. These grazing rates were ecosystems; and (c) to demonstrate how lotic meio-
reported for broad taxonomic groups and as discrete fauna are integrated within real benthic food webs.
snapshots, so that the functional role of lotic meio-
fauna remains under discussion.
Meiofaunal feeding habits
Since Pomeroy's study (1974) on oceanic food webs,
a broad theme in the understanding of microbial food
Detritus as food source
webs has been that of the trophic role of phagotrophic
protists. Protists graze microbial cells, remineralise Detritus is defined as the nonpredatory losses of
nitrogen and phosphorus bound in these prey, and organic carbon from any trophic level (i.e. egestion,
serve as a food source for higher trophic levels. Some excretion, secretion) or as the input from sources
experimental studies in lakes, however, reveals little external to the ecosystem that enter and cycle in the
top-down control by protozoans, particularly if the system such as allochthonous organic carbon (Wetzel
cladoceran Daphnia is abundant (Pace & Cole, 1994). et al., 1972). It is well known that detritus is of vital
Therefore, the overall significance of protozoan pre- importance for the nutrition of meiofaunal organisms
dation in regulating bacteria will vary among systems in sediments (Giere, 1993 and references therein).
and seasons. In streams, protists > 50 mm which fall Experimental work in marine systems has demon-
within the size range of meiofauna can be abundant strated that detritivorous meiofauna mostly utilise
(Sleigh, Baldock, & Baker, 1992; Schmid-Araya, 1994; bacterial biofilms, and not the detrital substrate itself
Eisenman, Traunspurger & Meyer, 1997). However, (Fenchel, 1970; Hargrave, 1972; Meyer-Reil & Faubel,
evidence of the trophic link between benthic Protozoa 1980). Furthermore, some members of the meiofauna
and higher metazoan consumers is only qualitative. such as ciliates (Fenchel, 1969), marine harpacticoids

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

 Trophic relationships of lotic meiofauna 151
(Carman & Thistle, 1985) and oligochaetes (Dash & C. Other laboratory experiments, however, have
Cragg, 1972) have been found to discriminate between shown that some harpacticoid species selected bacter-
various groups of bacteria and microfungi. ial C over diatom C when offered equal amounts of
In streams, fine particulate organic matter (FPOM) both C (Brown & Sibert, 1977).
is an important energy source due to the associated In marine systems, functional relations between
biofilm layer, which increases with sediment depth the structure of meiofauna mouth parts and the
particularly in gravel streams (Leichtfried, 1991). shape of bacteria have been demonstrated in detail
Significant relationships between amounts of inter- for nematodes (Jensen, 1987) and harpacticoids
stitial sediment and harpacticoid copepods and (Marcotte, 1984). Studies of marine organisms, and
nematodes have been found in colonisation experi- the very few examples of the freshwater meio-
ments within the hyporheic zone (Schmid-Araya, benthos, have shown that invertebrates not only
2000) These results can be attributed to passive take up particulate/fine organic matter, but also
particle-associated transport due to their feeding dissolved organic substances adsorbed to organic
habits within the hyporheic zone. particles (Meyer-Reil & Faubel, 1980). In lotic
Most of the permanent meiofauna, such as gastro- ecosystems, further estimates of grazing rate and
trichs, microturbellarians, rotifers, nematodes, small- bacterial/algal ingestion rate are needed, particularly
sized oligochaetes, cladocerans and harpacticoid in situ measurements.
copepods, are filter-feeders, suspension feeders, or
browsers (see Dole-Olivier et al., 2000; Kolasa, 2000;
Meiofauna as a food source
Ricci & Balsamo, 2000; Traunspurger, 2000). These
taxa feed on varying sizes of particles coated with Predation on meiofauna by other meiofaunal taxa
biofilm (fungi, diatoms, bacteria and their extracellu- Lotic meio-and macrofaunal predators feed on a
lar secretions). Few studies, however, have shown a wide variety of freshwater organisms, as well as fine
significant effect of meiofauna on detritally associated and ultrafine particulate organic matter and diatoms.
bacteria, although Perlmutter & Meyer (1991) demon- Table 1 summarises data on predator and prey
strated that the harpacticoid Attheyella spp. removed species for taxa inhabiting running waters. The
larger rod-shaped bacteria sufficient to reduce bacter- prey of large protozoans, microturbellarians, rotifers,
ial density and biomass. These experiments are the nematodes and oligochaetes are less well known
only one of this type for lotic meiofauna and the role than those of macroinvertebrates (Table 1). Clearly,
of many other taxa awaits investigation. predation by meiofaunal species is poorly studied in
Estimates of the ingestion rate of bacterial carbon by lotic systems. In lakes, there are accounts of rotifers
meiofauna are mainly available for marine taxa, with feeding on protozoans, and feeding on heterotrophic
fewer values for lotic meiofauna. Laboratory estimates and mixotrophic flagellates has been observed in
of Perlmutter & Meyer (1991) gave a range between culture conditions. Arndt (1993) found that some
0.03 and 0.47 mg of bacterial C ind±1 day±1 for rotifers could select heterotrophic flagellates that
Atheyella spp. (Copepoda: Harpacticoida) and their exhibit different `swimming' behaviour. Reports on
experiments demonstrated an effect of flow rate on rotifers feeding on ciliates are mainly for planktonic
bacterial production. Duncan, Schiemer & Klekowski species (Sanders & Wickham, 1993), and few benthic
(1974) published grazing rates of the bacteria-feeding species have been examined (Arndt, 1993). Further-
nematode Plectus palustris de Man of 0.032 ´ 10±3 h±1, more, Sorokin & Paveljeva (1972) estimated that the
while Admiraal et al. (1983) gave an average nema- predatory rotifer Asplanchna priodonta Gosse,
tode grazing rate on diatoms of 3.6 ´ 10±3 h±1. In situ removed 72% of the daily production of protozoan
estimates reported by Montagna (1984) showed that, biomass in Lake Dalnee. In stream ecosystems, field
during summer, the marine meiofauna (copepods, investigations on benthic rotifers feeding on flagel-
nematodes, ostracods) ingested 0.042 mg bacterial C lates, as well as their impact on ciliate production,
animal±1 day±1 and 0.53 mg algal C animal±1 day±1. are nonexistent.
During the winter, the same taxa ingested 0.53 mg of The food and feeding behaviour of cyclopoid
bacteria and 0.29 mg of algal C animal±1 day±1. In copepods have been studied in detail by Fryer
general these taxa ingested more algal C than bacterial (1957), and there is some other information of their

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152 J. M. Schmid-Araya and P. E. Schmid
Table 1 Lotic predators feeding on meiofauna

Predator Prey Reference

Protozoa
Heliozoa
Actinosphaerium Rotifera Hollowday (1949)
Ciliata
Condylostoma Rotifera Arndt (1993)
Dileptus Rotifera, three species; microturbellaria Sander & Wickhman (1993);
Schmid-Araya & Schmid (1995)
Trachelius Rotifera, three species Hollowday (1979); Schmid-Araya &
Schmid (1995)
Turbellaria
Geocentrophora Rotifera, four species Schmid-Araya & Schmid (1995)
Stenostomum Rhizopoda (Arcella) Schmid-Araya, Hildrew & Roberston
(unpublished)
Rotifera
Proales Rhizopoda (Rhadiophrys) Koste (1978)
Notommata Ciliophora Pourriot (1965, 1977)
Cephalodella Sessile Ciliophora; Rotifera, two species Pourriot (1965); Schmid-Araya & Schmid (1995)
Dicranophorus Ciliophora; Rhizopoda (Difflugia); Rotifera Spittler (1976); Koste (1978);
Schmid-Araya & Schmid (1995)
Aspelta Ciliophora Koste (1978)
Encentrum Ciliophora; Rhizopoda (Arcella); Rotifera, Koste (1978); Schmid-Araya &
four species Schmid (1995)
Nematoda
Prionchulus Rotifera, two species Schmid-Araya & Schmid (1995)
Mononchus Rotifera, two species Schmid-Araya, Hildrew & Roberston
(unpublished)
Anatonchus Rotifera, four species; Oligochaeta Schmid-Araya & Schmid 1995
Oligochaeta
Chaetogaster Bacillariophiceae; Protozoa (Ciliophora), SchoÈnborn (1984); Schmid-Araya &
13 species; Rotifera, seven species Schmid (1995)
Diptera
Chironomidae
Macropelopiini
Brundiniella Protozoa; Acari; Chironomidae; Tardigrada; Roback (1978);
Ostracoda; Microcrustacea
Procladius Protozoa; Gastrotricha; Oligochaeta; Roback (1969); Loden (1974); Baker &
Ephemeroptera; Ceratopogonidae; Microcrustacea Mc Machlan (1979); Kajak (1980)
Macropelopia notata Bacillariophiceae; Rotifera, 14 species; Ephemeroptera, Schmid-Araya & Schmid (1995)
(Meigen) two species; Plecoptera, two species; Chironomidae,
29 species; Ostracoda
Macropelopia goetghebueri Bacillariophiceae; Rhizopoda, five species; Rotifera, Schmid-Araya, Hildrew & Roberston
(Kieffer) 10 species; Oligochaeta; Chironomidae, eight species; (unpublished)
Tardigrada; Microcrustacea, three species
Apsectrotanypus Bacillariophiceae; Rhizopoda, four species; Rotifera, Schmid-Araya, Hildrew & Roberston
seven species; Oligochaeta, two species; Chironomidae, (unpublished)
six species; Microcrustacea two species
Pentaneurini
Ablabesmyia Oligochaeta; Rotifera; Chironomidae; Microcrustacea Loden (1974), Coffman & Ferrington (1984)
Conchapelopia pallidula Bacillariophiceae; Rotifera, 36 species Chironomidae, Schmid-Araya & Schmid (1997)
(Meigen) eight species; Tardigrada; Microscrustacea; Ostracoda
Conchapelopia viator Rhizopoda, two species; Rotifera, seven species Schmid-Araya, Hildrew & Roberston
(Kieffer) (unpublished)
Krenopelopia Rhizopoda; Rotifera, three species; Chironomidae Schmid-Araya, Hildrew & Roberston
(unpublished)

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 Trophic relationships of lotic meiofauna 153
Table 1 continued

Predator Prey Reference

Labrundinia Oligochaeta Loden (1974)

Nilotanypus Bacillariophiceae; Rotifera, 27 species; Chironomidae, Schmid-Araya & Schmid (1997)
12 species; Tardigrada; Microscrustacea; Ostracoda
Diptera
Chironomidae
Pentaneurini
Natarsia Chironomidae, two species Schmid-Araya, Hildrew & Roberston
(unpublished)
Paramerina Bacillariophiceae; Rotifera, two species; Chironomidae, one species Schmid-Araya & Schmid (1995)
Thienemannimyia. Laeta Bacillariophiceae; Rotifera, 10 species; Chironomidae, Schmid-Araya & Schmid 1995
(Meigen) three species; Tardigrada
T. Geijskesi (Goet.) Bacillariophiceae; Rotifera, 34 species; Chironomidae, Schmid-Araya & Schmid (1997)
22 species; Tardigrada; Microscrustacea
Trissopelopia longimana Bacillariophiceae; Rotifera, five species; Ephemeroptera, Schmid-Araya & Schmid (1995)
(Staeger) two species; Chironomidae, five species; Tardigrada; Ostracoda (calcareous stream)
T. Longimana (Staeger) Bacillariophiceae; Rhizopoda, four species; Rotifera, nine Schmid-Araya, Hildrew & Roberston
species; Nematoda, two species; Oligochaeta; (acid stream, unpublished)
Chironomidae, 10 species; Microcrustacea five species
Zavrelimyia signatipennis Bacillariophiceae; Protozoa; Oligochaeta; Rotifera, six Schmid-Araya & Schmid 1997
species; Tardigrada; Ostracoda
Zavrelimyia barbatipes Bacillariophiceae; Rhizopoda, four species; Rotifera, Schmid-Araya, Hildrew & Roberston
(Kieffer) 10 species; Oligochaeta; Chironomidae, three species; (unpublished)
Tardigrada; Microcrustacea, four species
Limoniidae
Pedicia Acari; Oligochaeta; Rotifera; Microcrustacea Crisp & Lloyd (1954); Schmid-Araya
& Schmid (1995)
Dicranota Oligochaeta Crisp & Lloyd (1954)
Limnophila Chironomidae; Oligochaeta; Nematoda, two species Crisp & Lloyd (1954); Schmid-Araya,
Hildrew & Roberston (unpublished)
Oxydiscus Rhizopoda Crisp & Lloyd (1954)
Plecoptera
Isoperla (1±2 mm) Bacilllariophiceae, two species; Rhizopoda; Schmid-Araya & Schmid (1995)
Oligochaeta; Rotifera, 15 species; Chironomidae,
eight species; Tardigrada
Dinocras (1±2 mm) Rotifera, five species; Chironomidae Schmid-Araya & Schmid (1995)
Chloroperla (3 mm) Rhizopoda; Rotifera; Chironomidae; Microcrustacea Schmid-Araya & Schmid (1995)
Siphonoperla torrentium Rhizopoda, seven species; Oligochaeta, two species; Schmid-Araya, Hildrew & Roberston
(4±6 mm) Acari; Rotifera, two species; Ephemeroptera; Plecoptera; (unpublished)
Chironomidae, four species; Microcrustacea; Ostracoda
Copepoda
Cyclopoida
Acanthocyclops Rotifera: 15 species; Microcrustacea, seven species Fryer (1957), Carney, Havens &
Bersier (1997)
Megacyclops Rotifera Fryer (1957), Schmid-Araya &
Schmid (1995)
Macrocyclops Microcrustacea Fryer (1957), Schmid-Araya, Hildrew
& Roberston (unpublished)
Trichoptera
Plectrocnemia Rhizopoda; Rotifera; Chironomidae, 11 species; Lancaster & Robertson, 1995;
Microcrustacea, four species Schmid-Araya, Hildrew & Roberston
(unpublished)
Megaloptera
Sialis Rhizopoda; Rotifera, two species; Chironomidae, Lancaster & Robertson, 1995;
nine species; Microcrustacea, two species Schmid-Araya, Hildrew & Roberston
(unpublished)

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154 J. M. Schmid-Araya and P. E. Schmid
feeding in stream systems (Table 1). The food includes In marine systems, the effect of macroinvertebrate
other meiofaunal taxa such as rotifers, microcrusta- predators upon meiofauna is still under debate.
ceans, dipteran larvae and oligochaetes, many of them Gerlach & Schrage (1969) demonstrated no substantial
larger than their copepod predators. impact of shrimps (Crangon crangon L.) upon meio-
Other meiofaunal predators include the nematode benthos, while Mc Intyre (1969) argued that the
genera Dorylaimus, Prionchulus, Anatonchus and Mono- impact of macrofaunal predation is less substantial
nchus, which are able to feed on protozoans, and all than expected. Bell & Coull (1978), however, sug-
types of meiofauna such as rotifers, oligochaetes, gested the opposite, although the initial meiofaunal
gastrotrichs, tardigrades, mites and other nematodes abundances in their experimental tanks were very
(Meyl, 1961). However, few field studies have explored variable leading to inconclusive results.
the diet of such groups in stream communities. In freshwaters, O'Doherty (1988) experimentally
Microturbellarians are known to exhibit a variety of removed macrofauna from areas of streambed and
feeding behaviours to consume bacteria, algae, proto- found a variable response of meiofaunal abundance,
zoans and invertebrates (Kolasa, 2000), although their suggesting that macrofauna affected meiofaunal den-
feeding habits are known mostly from lentic species sity to some degree. In a gravel stream, Schmid &
(Kolasa, 1991). The most common predatory meiofau- Schmid-Araya (1997) found that the impact of larval
nal oligochatete is the naidid Chaetogaster, which can tanypods upon meiofauna was low and that larvae
be cultured on a wide variety of ciliates (Taylor, 1980). were not selective in their feeding. Tanypod predation
SchoÈnborn (1984) found that Chaetogaster diastrophus amounted to 2.2% of combined prey density and prey
Gruithuisen showed prey selectivity and consumed consumption averaged 1.3 individuals per predator
72% of the annual production of ciliates on exposed individual per year. Analysis of the gut contents of
slides in the River Saale. three tanypod species in Broadstone Stream (Hildrew,
Townsend & Hasham, 1985), revealed that copepods
constituted less than 20% of the diet. Streambed
Predation on meiofauna by fish and macroinvertebrates
sediments are heterogeneous (Schmid, 1993) and the
Accounts of lotic fish and macroinvertebrates feeding
structural complexity could provide spatial refugia,
on meiofaunal taxa are few and scattered in the
reducing predator efficiency and the overall effect of
literature. Some studies have shown that marine fish
predators on prey (Schmid & Schmid-Araya, 1997).
such as plaice (Bregnalle, 1961) or salmon (Kaczynski
Furthermore Banse & Mosher (1980), reviewing the P/
et al., 1973; Sibert et al., 1977), do not distinctly deplete
B ratios across different animal phyla, concluded that
meiofaunal populations, while others argued the
turnover rates of marine meiofauna were lower than
opposite (Sibert, 1979). In gravel streams, 0 + bullhead
expected on the basis of their size, implying that these
Cottus gobio L. fed mainly on chironomids, whereas
organisms may be subject to low predation. Whether
2 + individuals took larger macroinvertebrates, such
this pattern also applies to freshwater meiofauna is
as plecopterans, trichopterans, simuliids and ephe-
still uncertain. Unfortunately, experiments on the
meropterans (Adamicka, 1991). In Southern English
effect of predation can only be designed for more
streams, the diet of underyearling of Brown trout
conspicuous groups, such as microcrustaceans,
(Salmo trutta L.) and Stone Loach (Noemacheilus
because soft-bodied taxa may be difficult to handle
barbatulus L.) included meiofauna (Rundle & Hildrew,
and manipulate. Another important consideration is
1992). Between 26 and 76% of the numbers of prey in
that macroinvertebrates such as insect predators have
the guts of Brown trout < 30 mm in length were
ontogenic changes throughout their life cycle, shifting
cyclopoids and chironomids, respectively, whereas up
their diet from small-to large-sized (Hildrew, Town-
to 80% were chironomid larvae in the guts of Stone
send, & Hasham, 1985; Schmid & Schmid-Araya,
Loach (see also discussion in Swan & Palmer, 2000). In
1997). Therefore the effect of predation upon the meio-
similar streams, we have found that Cottus gobio (size
and microfauna assemblages may be only seasonal.
range between 8 and 12 mm) feeds on diatoms,
Many predacious insects in streams are believed to
cyclopoid and harpacticoid copepods, cladocerans
begin as grazers/detritivores and shift to a carnivor-
and chironomids (Schmid-Araya, Robertson & Hil-
ous diet later in their life cycle (Anderson &
drew, unpublished).
Cummins, 1979). Others have demonstrated seasonal

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 Trophic relationships of lotic meiofauna 155
shifts within the same species (Malmqvist, SjoÈstroÈm & streams. Our results in a calcareous Austrian stream
Frick, 1991). In contrast to macroinvertebrates, meio- showed the opposite: I. difformis took a wider range of
faunal predators such as large ciliates, microturbellar- meiofaunal prey than did I. grammatica (Schmid-
ians, rotifers and small oligochaetes may or may not Araya & Schmid 1995). These divergent results
reveal ontogenetic shifts in prey choice through their could be a reflection of differences in species life
life cycles. cycles between different lotic ecosystems, or differ-
In standing waters, we know most of the diet of ences in prey available, particularly of meiofaunal
predatory chironomids through research on the genus size, between streams.
Procladius. Moore (1979)) found that P. denticulatus We also examined and identified the diet of small-
Sublette fed on first and second instars of several sized stonefly nymphs of Dinocras cephalotes (Curtis)
chironomid species and gastrotrichs (probably Stylo- and Chloroperla susemicheli (Zwick), which fed upon a
chaeta and Chaetonotus sp.). Procladius sp. fed mainly number of meiofaunal taxa among which rotifers
on microcrustaceans and chironomids (Dusoge, 1980), were the most abundant (Table 1). These results
while first to third instars larvae of Procladius bellus contrast to that of Lucy, Costello & Giller (1990),
(Loew) consumed detritus (particles between 1 and who reported mainly macrofaunal-size prey in the
15 mm), diatoms, rotifers, cladocerans and copepods diet of D. cephalotes and Perla bipunctata (Pictet).
(Sephton, 1987). Another tanypod predator Thiene- Though there is much qualitative information, there
mannimyia festiva Fittkau was found to consume are very few quantitative estimates of the role of
oligochaetes, copepods, chironomids and first and meiofauna in the diet of meio-and macro-inverte-
second instars of the caddisfly Polycentropus flavoma- brates. The data available indicate that meiofauna are
culatus (Pictet) in Lough Neagh (Tokeshi, 1991). an important component of the diet of lotic inverte-
In an acid stream, Hildrew et al. (1985) studied the brates at least during part of their life cycle. Perhaps
diet of three tanypod species and found mixed diet feeding on meiofauna enhances the survival and
of detritus, algae and animal prey such as copepods, growth of predatory and omnivorous macrofaunal
chironomids, plecopterans and mites. The work of taxa because of their nutritional value as food and
Schmid (1994), Schmid-Araya & Schmid (1995) and because their body size makes them available to early
Schmid & Schmid-Araya (1997) illustrated the instar larvae.
importance of soft-bodied meiofaunal taxa as the
main prey of larval tanypod Chironomidae. Further,
Integrating meiofauna in stream food webs
in a limestone gravel stream, three tanypod species
preyed upon 97 different species and instars ranging General food web considerations
between 75 mm and 6.5 mm (Schmid & Schmid- Food webs are networks of consumer±resource inter-
Araya, 1997). actions among a group of organisms, populations or
Lancaster & Robertson (1995) were the first to detail trophic units. Trophic interactions can be established
the occurrence of benthic microcrustaceans in the diet based on diet analyses performed on field-collected
of the alderfly Sialis fuliginosa Pictet and the caddisfly material, and additional behavioural feeding observa-
Plectrocnemia conspersa Curtis in an acid stream. tions and experiments. Food webs can be described
Further inspection of the diet of these predators, using all the constituent taxa where feeding interac-
particularly smaller instars, shows that testate amoeba tions are extrapolated into matrices with n x n species
(Protozoa: Rhizopoda) and rotifers are also taken as and food web properties (i.e. connectance, linkage
prey (Table 1). density) can be estimated. Another type of approach
Feminella & Stewart (1986) listed some meiofaunal is a functional one, however, where only the impor-
taxa within the diet of leaf-associated stoneflies, but tant species and feeding links are identified within the
did not resolve them to species level. Similarly community.
Malmqvist et al. (1991) found chironomids and crus- The basis of food web theory in freshwaters began
taceans in the diet of two Isoperla species (Plecoptera: by examining plankton (Lindeman, 1942) and con-
Perlodidae). They suggested that Isoperla grammatica tinued to develop extensively to: (a) illustrate biolo-
(Poda) ingest a greater diversity of prey than gical control by top predators (Brooks & Dodson,
I. difformis (Klapalek) in a wide range of Swedish 1965; Carpenter, Kitchell & Hodgson, 1985); and (b)

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

156 J. M. Schmid-Araya and P. E. Schmid
In stream ecosystems, the role of the microbial loop
was first envisaged by Cummins (1974). Much later,
Meyer (1994) attributed the difference between the
riverine and the marine microbial loops to allochtho-
nous sources of carbon. In addition, macroinverte-
brate consumers that feed directly on bacteria in
running water are very abundant and therefore there
should be fewer trophic links between bacteria and
top consumers (Fig. 1). Conversely, manipulative
experiments of fish demonstrated the effect of a
trophic cascade in a temperate stream dominated by
filamentous algae (Power, 1990). Roach and juvenile
steelhead consumed predatory insects, while fish fry
suppressed algivorous chironomids (sensu Power,
1990), switching the substratum from open to well
covered by plants. Results from such experiments
suggest that streams are systems with low complexity.
However, when meiofauna are included into stream
species lists, the benthic species richness increases
(Schmid-Araya & Schmid, 1995; Hakenkamp &
Palmer, personal communication). A higher number
of species increases the potential for buffering
processes, and thus the possibility for trophic cas-
Fig. 1 Diagram of a lotic food web exemplifying sources and
cades decreases (Hildrew, 1992; Strong, 1992).
major pathways of organic carbon (adapted from Meyer, 1994).
Dotted lines indicate flows that are part of the microbial loop in
lotic systems.
The role of meiofauna within stream food webs

Although food-web theory has existed for decades,

suggest that a trophic cascade (fish-zooplankton- food web descriptions in streams have lagged behind
phytoplankton) extends to heterotrophic microbes those for other habitat types, and the issue of the role
(Stockner & Porter, 1988). of small metazoans is generally unresolved. River and
However, the definition of a food web requires stream food webs were included within the theore-
setting some habitat boundary. Thus, spatial organi- tical analyses of Briand (1983), Briand & Cohen (1987)
sation within a lake (i.e. profundal, littoral and pelagic and Sugihara, Schoenly & Trombla (1989), although
zones) may have important influences on the way these were highly over-simplified and based on
species interact and result in functionally distinct food macroinvertebrates (i.e. > 500 mm), and it was subse-
webs (Warren, 1989). The early work of Wiszniewski quently suggested that these systems were species
(1947), studying freshwater psammon (the commu- poor. These compilations included only nine webs
nity inhabiting sandy beaches, mostly of meiofaunal from streams and rivers and the highest number of
size), was among the first to make depictions of the species detected was 60 from a compilation of three
flows of energy and/or material throughout the streams (Table 2).
community and its relationship to the pelagic. In the The stream web of Hildrew et al. (1985) included
marine plankton, the proposed carbon budget model some organisms temporarily of meiofaunal size (i.e.
of Pomeroy (1979) highlighted problems with the Chironomidae), and this was reflected in a higher
application of the trophic level concept. The high proportion of intermediate species. Lancaster &
degree of interconnection among the detrital pathway, Robertson (1995) revisited the same web with an
omnivory and microbial processes belie the validity of improved taxonomic resolution and demonstrated
the Lindeman model trophic organisation (Ducklow, that meiofauna in the diet of macroinvertebrates
1994). changed the values of connectance, predator-prey

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 Table 2 Food web properties of stream/river ecosystems

Food web statistic Aire, Nidd, Morgan's Deep Doe Run Duffin Oberer
Wharfe Dee Clydach Rheidol Thames Cam Creek Creek UT KY Creek Broadstone Seebach

19291 19491 19491 19502 19722 19482 19671,2 19731 19671 19963 19854 19955 19986 19977
Number of species, S or web size 60 34 ? 18 10 18 13 18 11 32±39 24 33 130 166

Species proportions
Top species (T) 1.29 0.41 0.28 ± ± ± 0.25 0.33 0.18 0.41±0.78 0.17 ± 0.07 0.10
Intermediate (I) 0.32 0.32 0.48 ± ± ± 0.63 0.50 0.64 0.03±0.43 0.71 ± 0.85 0.86

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

Basal (B) 0.57 0.27 0.24 ± ± ± 0.13 0.17 0.18 0.15±0.19 0.12 ± 0.08 0.04
Predator/prey ratio 3.08 1.25 1.05 ± ± ± 1.17 1.25 1 0.00±0.07 0.13 0.21 0.40 0.20
Maximum chain length 4 ± 4 4 4 4 4 3 4 ± 4 5 ± ±
Mean chain length 2.35 ± 2.35 3.16 2.93 2.89 2.72 2.33 2.83 ± 3.40 4.6 ± ±
Connectance (C = L/S2; Martinez, 1991) ± ± ± ± ± ± ± ± ± 0.19±0.20 0.25 0.23 0.09 0.07
Linkage density (d=L/S) ± ± ± ± (1.80) (1.78) (2.68) ± ± 3.16±3.74 2.5 3.7 5.6 5.8
SC 3.66 3.12 3.66 ± ± ± 3.92 3.0 2.73 ± 5.3 7.59 11.2 11.8
1
Sugihara, Schoenly & Trombla (1989).
2
Briand & Cohen (1987).
3
Tavares-Cromar & Williams (1996).
4
Hildrew et al. (1985).
5
Lancaster & Robertson (1995).
6
Schmid-Araya, Roberston & Hildrew (unpublished).
7
Schmid (unpublished).
Trophic relationships of lotic meiofauna
157
158 J. M. Schmid-Araya and P. E. Schmid

Fig. 2 Feeding relationships in the benthic food web of the acid stream Broadstone in South England during summer 1996 and spring
1997. The y-axis represents body length of the different taxa, while circle size indicates species richness. Horizontal dotted lines delimit
the boundaries of meiofaunal sizes. Li, Diptera, Limoniidae; TRI, Trichoptera; TE, Terrestrial; SI, Sialis; OLI, Oligochaeta; CE, Diptera,
Ceratopogonidae; SM, Diptera, Simuliidae; PLE, Plecoptera; CO, Coleoptera; AC, Acari; CHI, Diptera, Chironomidae; TU, Turbellaria;
NE, Nematoda; OS, Ostracoda; CY, Cyclopoida; CL, Cladocera; HA, Harpacticoida; RO, Rotifera; TA, Tardigrada; PLEG, plecopteran
eggs; TUEG, turbellarian eggs; PR, Protozoa; DI, Diatoms; BAC, Bacteria; FPOM, fine particulate organic matter; CPOM, coarse
particulate organic matter.

ratio and the fraction of intermediate species. Other also improved by resolving specifically the meiofauna
recent data listed 49 species in an intermittent stream in the diet of macroinvertebrates. There was a decrease
in Australia (Closs & Lake, 1994), where the meio- in the fraction of top and basal species, while the
fauna included 11 Chironomidae and five microcrus- proportion of intermediate species increased. Conse-
tacean species. Fewer species were found and quently, the predator-prey ratio, linkage density and
analysed in the food web of Duffin Creek in Canada linkage complexity increased with species richness,
(Tavares-Cromar & Williams, 1996). These studies mainly attributed to the meiofauna.
examined either the spatial, or temporal, variation of Our own observations and recent quantification of
the food web; organic detritus was the primary the gut contents of major consumers of macro-and
resource utilised by all nonpredatory species in the meiobenthos (Schmid & Schmid-Araya, 1997) showed
community. In Duffin Creek, time-specific webs that many stream invertebrates feed on meiofauna.
differed from a summary web in terms of the number The trophic position of meiofauna has probably not
of links, number of species, number of top and been well understood. For example, benthic rotifers
intermediate species, and linkage density. can occupy several trophic roles: herbivores (i.e.
Including the meiofauna the Broadstone Stream web Proales, Euchlanis), microbial feeders (most bdelloids),
(Table 2) increased the number of total species and omnivores including omnivorous predators (i.e.
therefore changed food web statistics. The food web of Dicranophorus) feeding on other larger ciliates and
a calcareous gravel stream in Austria (Table 2) was rotifers (Table 1). Another role for rotifers in the

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

 Trophic relationships of lotic meiofauna 159
microbial web, which may apply to most meiofaunal experiments. The question of how microbial growth
groups, is that they indirectly reduce populations of and nutrient uptake rate are affected by meiofauna,
algae, bacteria and protozoans promoting microbial also needs to be addressed.
activity (Arndt, 1993). In order to evaluate trophic interactions within the
Figure 2 shows the summer 96 and spring 97 food lotic meiofauna we need to consider temporal and
web of the Broadstone Stream. Seasonal variation in spatial dynamics and require a better knowledge of
these food webs is similar to that found by Closs & species composition, population interactions, densi-
Lake (1994) and Tavares-Cromar & Williams (1996). ties and growth dynamics. Understanding ecosystem
From a trophic perspective, however, the role of aspects, such as the processing of detritus, nutrient
rotifers, chironomids, protozoans (Rhizopoda:Testa- recycling and nutrient budgets, requires that the role
cea) and oligochaetes as food resource increases of individual species is clarified, as their contribution
during the summer. In spring 1997, when fewer to these processes may vary dramatically.
meiofaunal species occurred, diets shift mainly to the
temporary meiofauna, such as chironomids, and to
macroinvertebrates, such as plecopterans, with fewer Acknowledgments
rotifers, harpacticoids and protozoans (Fig. 2). Here, The study began in Austria, supported by the funds of
diet changes in response to a seasonal shift in the the Austrian Fonds zur FoÈrderung der wissenschaf-
availability of food resources. This type of species tlichen Forschung (FFWF-Projects 8007-BIO and
oriented approach within the food web clearly differs P8035-BIO). We thank members of the Biological
from the functional approach used by Meyer (1994). Station Lunz including Prof G. Bretschko, Dr M.
Taxonomic distinction is important, because captur- Leichtfried, Mrs E. Kronsteiner, Mag. Franz Wagner
ing food and foraging depends on the body structure and Mr E. Lanzenberger. The study of Broadstone
and body plan of the predator. In addition, the Stream is part of a major research supported by NERC
feeding biology differs with age and intraspecific Grant GR2/10548 awarded to Prof. A. G. Hildrew and
differences in resource use between age groups will Dr Anne Robertson.
occur where invertebrates have several developmen-
tal stages.
References
Conclusion Adamicka P.S. (1991) A food schedule for Cottus gobio L.
(Pisces) in Oberer Seebach, Ritrodat-Lunz study area,
There is still a limited knowledge of meiofaunal
Austria. Verhandlungen der Internationalen Vereinigung
trophic relationships in streams. This lack of informa- fuÈr Theoretische und Angewandte Limnologie, 24, 1941±
tion has been confounded by lumping the meiofauna 1943.
as a single trophic group linked to all trophic Admiraal W., Bouwman L.A., Hoekstra L. & Romeyn K.
compartments. (1983) Qualitative and quantitative interactions be-
It is becoming clear that the trophic importance of tween mycrophytobenthos and herbivorous meiofauna
meiofauna is wider and more intricate than expected. on brackish intertidal mudflat. Internationale Revue der
Many meiofauna, macroinvertebrates and fish seem to Gesamten Hydrobiologie, 68, 175±191.
rely on meiofauna groups as food, but while there are Anderson N.H. & Cummins K.W. (1979) Influences of
several qualitative studies of diet, quantitative esti- diet on life histories of aquatic insects. Journal of the
Fisheries Research Board Canada, 36, 335±342.
mates of predation on meiofauna in the field are few.
Arndt H. (1993) Rotifers as predators on components of
Estimates of macrofauna feeding rates on meiofauna
the microbial web (bacteria, heterotrophic flagellates,
are needed. In addition, these estimates may vary
ciliates) ± a review. Hydrobiologia, 255/256, 231±246.
among streams, depending on the meiofaunal species Baker A.S. & McMachlan A.J. (1979) Food preferences in
richness and their respective densities. It is clear that Tanypodinae larvae (Diptera: Chironomidae). Hydro-
further investigations on the effects of lotic meiofauna biologia, 62, 283±288.
upon bacterial production and/or biofilm compo- Banser K. & Mosher S. (1980) Adult body mass and
nents are also needed, including both comparative annual production/biomass relationships of field
studies of ecologically contrasting systems and field populations. Ecological Monographs, 50, 355±379.

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

160 J. M. Schmid-Araya and P. E. Schmid
Bell S.S. & Coull B.C. (1978) Field evidence that shrimp adult females of the benthic nematode, Plectus palustris
predation regulates meiofauna. Oecologia (Berlin), 35, De Man 1880. Polska Archiwum Hydrobiologii, 21, 249±
141±148. 258.
Borchardt M.A. & Bott T.L. (1995) Meiofaunal grazing of Dusoge K. (1980) The occurrence and role of the
bacteria and algae in a Piedmont stream. Journal of the predatory larvae of Procladius Skuse (Chironomidae,
North American Benthological Society of, 14, 278±298. Diptera) in the benthos of Lake SÂniardwy. Ekologia
Bregnalle F. (1961) Plaice and flounder as consumers of Polska, 28, 155±186.
the microscopic bottom fauna. Meddelelser Fra Dan- Eisenmann H., Traunspurger W. & Meyer E.I. (1997) A
marks Fiskeri-Og Havundersùgelser, 3, 133±182. new device to extract sediment cages colonized by
Briand F. (1983) Environmental control of food web microfauna from coarse gravel river sediments. Archiv
structure. Ecology, 64, 253±263. fuÈr Hydrobiologie, 139, 547±561.
Briand F. & Cohen J.E. (1987) Environmental correlates of Escavarage V., Garcia M.E. & Castel J. 1989) The
food chain length. Science, 238, 956±960. distribution of meiofauna and its contribution to
Brooks J.L. & Dodson S.I. (1965) Predation, body size, detritic path ways in tidal flats (Archachon Bay,
and composition of the plankton. Science, 150, 28±35. France). Scientia Marina, 53, 551±559.
Brown T.J. & Sibert J.R. (1977) The food of some benthic Feminella J.M. & Stewart K.W. (1986) Diet and predation
harpacticoid copepods. Journal of the Fisheries Research by three leaf associated stoneflies (Plecoptera) in an
Board Canada, 34, 1028±1031. Arkansas mountain stream. Freshwater Biology, 16, 521±
Carman K.R. & Thistle D. (1985) Microbial loop 538.
partitioning by three species of benthic copepods. Fenchel T. (1969) The ecology of the marine microbe-
Marine Biology, 88, 143±148. nthos. IV. Structure and function of the benthic
Carney H.J., Havens K.E. & Bersier L.F. (1997) Nonlinear ecosystem, its chemical and physical factors and the
scale dependence and spatiotemporal variability in microfauna communities with special reference to the
planktonic food webs. Oikos, 79, 230±240. ciliate Protozoa. Ophelia, 6, 1±182.
Carpenter S.R., Kitchell J.F. & Hodgson J.R. (1985) Fenchel T. (1970) Studies on the decomposition of
Cascading trophic interactions and lake productivity. organic detritus derived from the turtlegrass Thalassia
Bioscience, 35, 634±639. testudinum. Limnology and Oceanography, 15, 14±20.
Closs G.P. & Lake P.S. (1994) Spatial and temporal Findlay S. & Tenore K.R. (1982) Effect of a free-living
variation in the structure of an intermittent-stream marine nematode (Diplolaimella chitwoodi) on detrital
food web. Ecological Monographs, 64, 1±21. carbon mineralization. Marine Ecology Progress in Series,
Coffman W.P. & Ferrington L.C. Jr (1984) Chironomidae. 8, 161±166.
An Introduction to the Aquatic Insects of North America Fryer G. (1957) The feeding mechanism of some fresh-
(Eds R.W. Merrit and K.W. Cummins), pp. 551±652. water Cyclopoid Copepods. Proceedings of the Zoological
Kendall/Hunt Publishing Company, Iowa. Society of London, 129, 1±25.
Crisp G. & Lloyd Ll. (1954) The community offsets in a Gerlach S.A. & Schrage M. (1969) Freilebende nematoden
patch of woodland mud. Transactions of the Royal als Nahrungs der Sandgarnele Crangon crangon. Ex-
Entomological Society of London, 105, 269±276. perimentelle Untersuchungen uÈber die Bedeutung der
Cummins K.W. (1974) Structure and function of stream Meiofauna als Nahrung fuÈr das marine Makrobenthos.
ecosystems. Bioscience, 24, 631±641. Oecologia, 2, 362±375.
Dash M.C. & Cragg J.B. (1972) Selection of microfungi by Giere O. (1993) Meiobenthology. The Microscopic Fauna in
Enchytraeidae (Oligochaeta) and other members of the Aquatic Sediments Springer-Verlag, Berlin.
soil fauna. Pedobiologia, 12, 282±286. Hakenkamp C.C. & Morin A. (2000) The importance of
De Morais L.T. & Bodiu J.Y. (1984) Predation on meiofauna to lotic ecosystem functioning. Freshwater
meiofauna by juvenile fish in a Western Mediterranean Biology, 44, 165±175.
flatfish nursery. Marine Biology, 82, 209±215. Hargrave B.T. (1972) Aerobic decomposition of sediment
Dole-Olivier M.J., Galassi D.M.P., Marmonier P. & and detritus as a function of particle surface area and
Creuze des ChaÃtellier M. (2000) The biology and organic content. Limnology and Oceanography, 17, 583±
ecology of lotic microcrustaceans. Freshwater Biology, 596.
44, 63±91. Hildrew A.G., Townsend C.R. & Hasham A. (1985) The
Ducklow H.W. (1994) Modeling the microbial food web. predatory Chironomidae of an iron-rich stream: feed-
Microbial Ecology, 28, 303±319. ing ecology and food web structure. Ecological En-
Duncan A., Schiemer F. & Klekowski R.Z. (1974) A tomology, 10, 403±413.
preliminary study of feeding rates on bacterial food by Hildrew, A.G. (1992) Food web and species interactions.

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

 Trophic relationships of lotic meiofauna 161
The Rivers Handbook (Eds P. Calow and G.E. Petts), pp. cephalotes and Perla bipunctata (Plecoptera, Perlidae)
309±330. Blackwell Scientific, Oxford. in a South-West Irish stream. Aquatic Insects, 12, 199±207.
Hollowday E.D. (1949) On the capture of plankton Malmqvist B., SjoÈstroÈm P. & Frick K. (1991) The diet of
Rotifera as food by heliozoan Actinosphaerium eichhorni. two species of Isoperla (Plecoptera: Perlodidae) in
Journal of Quekett Microscopical Club, 4, 362±363. relation to season, site, and sympatry. Hydrobiologia,
Hollowday E.D. (1979) The capture and ingestion of the 213, 191±203.
plankton rotifer Asplanchna priodonta Gosse by the Marcotte M. (1984) Behaviourally defined resources and
holotrichous ciliate Trachelius. Microscopy, 33, 535±538. speciation in Tisbe (Copepoda: Harpacticoida). Journal
Jensen P. (1987) Feeding ecology of free-living aquatic of Crustacean Biology, 4, 404±416.
nematodes. Marine Ecology Progress in Series, 35, 187± Martinez N. (1991) Artifacts or attributes? effects of
196. resolution on the Little Rock Lake food web. Ecological
Kaczynski V.W., Feller R.J., Clayton J. & Gerke R.J. (1973) Monographs, 61, 367±392.
Trophic analysis of juvenile pink and chum salmon Mc Intyre A.D. (1969) Ecology of marine meiobenthos.
(Oncorhynchus gorbuscha and O. keta) in Puget Sound. Biological Reviews, 44, 245±290.
Journal of the Fisheries Research Board Canada, 30, 1003± Meyer J.L. (1994) The microbial loop in flowing waters.
1008. Microbial Ecology, 28, 195±199.
Kajak Z. (1980) Role ofvertebrate predators (mainly Meyer-Reil L.-A. & Faubel A. (1980) Uptake of organic
Procladius sp.) in benthos. Chironomidae: Ecology, matter by meiofauna organisms and interrelationships
Systematics, Cytology, and Physiology (Ed. D. Murray), with bacteria. Marine Ecology Progress in Series, 3, 251±
pp. 339±348. Pergamon Press, New York. 256.
Kasimir G. (1990) Mikrobiologische Untersuchungen im Meyl A.H. (1961) FadenwuÈrmer (Nematoden). EinfuÈh-
Lunzer Seebach. Jahresbericht Biologische Station Lunz, rung in die Kleinlebewelt. Franckh.sche-Verlagshan-
12, 55±69. dlung, W. Keller, Stuttgart.
Kolasa J. (1991) Turbellaria. Ecology and Classification of Montagna P.A. (1984) In situ measurements of meio-
North American Freshwater Invertebrates, (Eds J.H. Thorp benthic grazing rates on sediment bacteria and edaphic
and A.P. Covich), pp. 145±163. Academic Press, New diatoms. Marine Ecology Progress in Series, 18, 119±130.
York. Moore J.W. (1979) Some factors influencing the distribu-
Kolasa J. (2000) The biology and ecology of lotic tion, seasonal abundance and feeding of subarctic
microturbellarians. Freshwater Biology, 44, this issue. Chironomidae (Diptera). Archiv fuÈr Hydrobiologie, 85,
Koste W. (1978) Rotatoria. Die RaÈdertiere Mitteleuropas. 302±325.
GebruÈder Borntraeger, Berlin. O'Doherty E.C. (1988) The ecology of meiofauna in an
Lampert W. (1978) Release of dissolved organic carbon Appalachian headwater stream. PhD Dissertation, Uni-
by grazing zooplankton. Limnology and Oceanography, versity of Georgia.
23, 831±834. Orcutt J.D. & Pace M.L. (1984) Seasonal dynamics of
Lancaster J. & Robertson A. (1995) Microcrustacean prey rotifers and crustacean zooplankton populations in a
and macroinvertebrate predators in a stream food web. eutrophic monomictic lake with a note on rotifer
Freshwater Biology, 34, 123±134. sampling. Hydrobiologia, 119, 73±80.
Leichtfried M. (1991) POM in a gravel stream (Ritrodat- Pace M.L. & Cole J.J. (1994) Comparative and experi-
Lunz Study Area, Austria, Europe). Verhandlungen der mental approaches to top-down and bottom-up reg-
Internationalen Vereinigung fuÈr Theoretische und Ange- ulation of bacteria. Microbial Ecology, 28, 181±193.
wandte Limnologie, 24, 1921±1925. Pace M.L. & Orcutt J.D. (1981) The relative importance of
Lindeman R.L. (1942) The trophic-dynamic aspect of protozoans, rotifers, and crustaceans in a freshwater
ecology. Ecology, 23, 399±418. zooplankton community. Limnology and Oceanography,
Loden M. (1974) Predation by chironomid (Diptera) 26, 822±830.
larvae on oligochetes. Limnology and Oceanography, 19, Perlmutter D.G. & Meyer J.L. (1991) The impact of a
156±159. stream-dwelling harpacticoid copepod upon detritally-
Lodge D.M., Barko J.W., Strayer D., Melack J.M., associated bacteria. Ecology, 72, 2170±2180.
Mittelbach G.G., Howarth R.W., Menge B. & Titus Pomeroy L.R. (1974) The ocean's food web, a changing
J.E. (1988) Spatial heterogeneity and habitat interac- paradigm. Bioscience, 24, 499±504.
tions in lake commmunities. Complex Interactions in Pomeroy L.R. (1979) Secondary production mechanisms
Lake Communities (Ed. S.R. Carpenter), pp. 181±208. of continental shelf communities. Ecological Processes in
Springer-Verlag, New York. Coastal and Marine Systems (Ed. R.J. Livingston), pp.
Lucy F., Costello M.J. & Giller P.S. (1990) Diet of Dinocras 163±186. Plenum Press, New York.

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

162 J. M. Schmid-Araya and P. E. Schmid
Porter K.G., Paerl H., Hodson R., Pace M.L., Priscu J., Schmid-Araya J.M. & Schmid P.E. (1995) Preliminar
Riemann B., Scavia D. & Stockner J. (1988) Microbial results on diet of stream invertebrates species: the
interactions in lake food webs. Complex Interactions in meiofaunal assemblages. Jahresbericht Biologische Station
Lake Communities (Ed. S.R. Carpenter), pp. 209±227. Lunz, 15, 23±31.
Springer-Verlag, New York. SchoÈnborn W. (1984) The annual energy transfer from the
Pourriot R. (1965) Recherches sur l'ecologie des rotiferes. communities of Ciliata to the population of Chaetogaster
Vie et Millieu, (Suppl. 21), 1±224. diastrophus (Gruithuisen) in the River Saale. Limnologi-
Pourriot R. (1977) Food and feeding habits of Rotifera. ca, 16, 15±23.
Archiv fuÈr Hydrobiologie, 8, 243±260. Sephton T.W. (1987) Some observations on the food of
Power M.E. (1990) Effects of fish in River food webs. larvae of Procladius bellus (Diptera: Chironomidae).
Science, 250, 411±415. Aquatic Insects, 9, 195±202.
Ricci C. & Balsamo M. (2000) The biology and ecology of Sibert J.R. (1979) Detritus and juvenile salmon production
lotic rotifers and gastrotichs. Freshwater Biology, 44, 15± in the Nanaimo Estuary: II. Meiofauna available as food
28. for juvenile chum salmon (Oncorhynchus keta). Journal of
Rieman F. & Schrage M. (1978) The mucus-trap hypoth- the Fisheries Research Board Canada, 36, 497±503.
esis of feeding of aquatic nematodes and implications Sibert J.R., Brown T.J., Healey M.C., Kask B.A. &
for biodegradation and sediment texture. Oecologia, 34, Nauman R.J. (1977) Detritus- based food webs:
75±88. exploitation by juvenile chum salmon (Oncorhynchus
Roback S.S. (1969) Notes on food of Tanypodinae larvae. keta). Science, 196, 649±650.
Entomological News, 80, 13±18. Sleigh M.A., Baldock B.M. & Baker J.H. (1992) Protozoan
Roback S.S. (1978) The immature chironomids of the communities in chalk streams. Hydrobiologia, 248, 53±64.
eastern United States III. Tanypodinae, Anatopyniini, Sorokin Y.I. & Paveljeva E.B. (1972) On the quantitative
Macropelopiini and Natarsiini. Proceedings of the characteristics of the pelagic ecosystems of Dalnee
Academy of Natural Sciences of Philadelphia, 129, 151± Lake (Kamchatka). Hydrobiologia, 40, 519±552.
202. Spittler P. (1976) BeitraÈge zur Kenntnis der Nahrung-
Robertson A.L., Rundle S.D. & Schmid-Araya. J.M. (2000) sauswahl von Zooplanktern eutropher KuÈstengewaÈs-
Putting the meio- into stream ecology: current findings ser. Wissenschaftiche Zeitschrift UniversitaÈt Rostock,
and future directions for lotic meiofaunal research. Mathematik und Natur. R , 25, 305±310.
Freshwater Biology, 44, 177-183. Stockner J. & Porter M.L. (1988) Microbial food webs in
Rundle S.D. & Hildrew A.G. (1992) Small fish and small freshwater planktonic ecosystems. Complex Interactions
prey in the food webs of some southern English in Lake Communities (Ed. S.R. Carpenter), pp. 69±83.
streams. Archiv fuÈr Hydrobiologie, 12, 25±35. Springer-Verlag, New York.
Sanders R.W. & Wickham S.A. (1993) Planktonic proto- Strong D.R. (1992) Are trophic cascades all wet?
zoa and metazoa: predation, food quality and popula- Differentitation and donor-control in speciose ecosys-
tion control. Marine Microbial Food Webs, 7, 197±223. tems. Ecology, 73, 747±754.
Schmid P.E. (1993) Random patch dynamics of larval Sugihara G., Schoenly K. & Trombla A. (1989) Scale
Chironomidae (Diptera) in the bed sediments of a invariance in food web properties. Science, 245, 48±52.
gravel stream. Freshwater Biology, 30, 239±255. Swan C.M. & Palmer M.A. (2000) What drives small-
Schmid P.E. (1994) Is prey selectivity by predatory scale spatial patterns in lotic meifauna communities?
Chironomidae a random process ? Verhandlungen der Freshwater Biology, 44, 109±121.
Internationalen Vereinigung fuÈr Theoretische und Ange- Tavares-Cromar A.F. & Williams D.D. (1996) The
wandte Limnologie, 25, 1656±1660. importance of temporal resolution in food web
Schmid P.E. & Schmid-Araya J.M. (1997) Predation on analysis: Evidence from a detritus-based stream.
meiobenthic assemblages: resource use of a tanypod Ecological Monographs, 66, 91±113.
guild (Chironomidae, Diptera) in a gravel stream. Taylor W.D. (1980) Observations on the feeding and
Freshwater Biology, 38, 67±91. growth of the predacious oligochaete Chateogaster langi
Schmid-Araya J.M. (1994) Temporal and spatial dis- on ciliated Protozoa. Transactions of the American
tribution of benthic microfauna in sediments of a Microscopy Society of, 99, 360±367.
gravel streambed. Limnology and Oceanography, 39, Tenore K.R. & Rice D.L. (1980) A review of trophic
1813±1821. factors affecting secondary production of deposit-
Schmid-Araya J.M. (2000) Invertebrate recolonization feeders. Marine Benthic Dynamics (Eds K.R. Tenore
patterns in the hyporheic zone of a gravel stream. and B.C. Coull), pp. 325±340. University of South
Limnology and Oceanography (in press). Carolina Press, Columbia.

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163

 Trophic relationships of lotic meiofauna 163
Tenore K.R., Tietjen J.H. & Lee J.H. (1977) Effect of Wetzel R.G., Rich P.H., Miller M.C. & Allen H.L. (1972)
meiofauna on incorporation of aged, Zostera marina, Metabolism of dissolved and particulate detrital
detritus by the polychaete Nephthys incisa. Journal of the carbon in a temperate hard-water lake. Memorie Dell9
Fisheries Research Board Canada, 34, 563±567. Istituto Italiano Di Idrobiologia, 29, 185±243.
Tokeshi M. (1991) On the feeding habits of Thienemanni- Wiszniewski J. (1947) Remarques relatives aux re-
myia festiva (Diptera: Chironomidae). Aquatic Insects, cherches recentes sur le psammon d'eaux douces.
13, 9±16. Archiwum Hydrobiologii Rybactwa, 13, 7±36.
Warren P.H. (1989) Spatial and temporal variation in
the structure of a freshwater food web. Oikos, 55, 299± (Manuscript accepted December 1999)
311.

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 149±163