RATES of METAZOAN MEIOFAUNAL MICROBIVORY : a REVIEW Paul Montagna

RATES OF METAZOAN MEIOFAUNAL MICROBIVORY : A REVIEW Paul Montagna

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Paul Montagna. RATES OF METAZOAN MEIOFAUNAL MICROBIVORY : A REVIEW. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 1995, pp.1-9. hal- 03051016

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RATES OF METAZOAN MEIOFAUNAL MICROBIVORY : A REVIEW

PAUL A. MONTAGNA The University of Texas at Austin, Marine Science Institute, P.O. Box 1267, Port Aransas, Texas 78373 U.S.A.

BACTERIES RÉSUMÉ - La méiofaune consomme des Bactéries, des microalgues, des Proto- MICROALGUES zoaires, du matériel détritique et d'autres méiobenthontes. Elle peut également ab- NUTRITION sorber de la matière organique dissoute. L'objet de cet article de synthèse concerne RÉPONSE FONCTIONNELLE la méiofaune microphage, et en particulier la prédation sur les Bactéries et les microalgues par les Nématodes et les Harpacticoïdes. La plupart des études utilisent les techniques radioisotopiques. Elles se divisent en deux catégories : celles qui envisagent d'élucider la biologie de la nutrition de la méiofaune, et celles qui cherchent à évaluer l'impact de l'importance de la méiofaune dans le recyclage du carbone. La méiofaune broute (sélectionne) les petites particules de la biomasse microbienne. Le taux de broutage de la méiofaune augmente lorsque l'abondance de la nourriture bactérienne disponible s'accroit. C'est une réponse fonctionnelle que les modèles d'optimisation prédisent. La méiofaune présente également des taux de consommation différents selon les sources de nourriture. Il existe des dif- férences ontogénétiques du taux de broutage et de sélection. Ces différences in- tragénériques sont faibles. Les modes de nutrition varient avec les diverses phases du cycle de vie. En dépis d'une forte variabilité d'un point à l'autre du globe, le taux moyen de broutage de la méiofaune est de 0,01 • h1, ce qui représente 1% par heure de la biomasse des hétérotrophes et des autotrophes. Ainsi, la méiofaune a un impact global significatif sur tous les processus faisant intervenir des micro- bionthes.

BACTERIA ABSTRACT - Metazoan meiofauna eat bacteria, microalgae, protozoans, détritus, MICROALGAE and other meiofauna. They also have the ability to absorb dissolved organic matter. FEEDING The focus of this review is on meiofaunal microbivory, particularly the use of FUNCTIONAL RESPONSES bacteria and microalgae by nématodes and harpacticoids. Most of the studies utilize radioisotope techniques. The studies fall into two catégories : those done to elu- cidate meiofaunal feeding biology, and those done to assess the impact and importance of meiofauna in carbon cycling. Meiofauna graze on (i.e., select) small particles of microbial biomass. Meiofaunal grazing rates increase when offered increased abundances of microbial food. This is a functional response predicted by optimization models. Meiofauna also have différent grazing rates on différent species of food. Ontogenetic grazing rate and sélection différences exist. The évi- dence for intrageneric différences in grazing rates is weak. Différences of feeding modes exist with différent life history stages. There is much variability from site to site Worldwide, but on average meiofauna graze at a rate of 0.01 h ', or 1% of the standing stock of both heterotrophs and autotrophs per hour. Therefore, meiofauna have a significant global impact on microbially mediated processes.

INTRODUCTION solid feeders that either eat or clean whole particles (Marcotte, B.M. 1977, Ph.D. Thesis, Dalhousie University, 212 pp., described in Hicks During the 1970's, little was known about how, and Coull, 1983). There are also four nematode what, and how much meiofauna consumed feeding groups : deposit feeders, epistrate feeders, (Fenchel, 1978; Coull and Bell, 1979). A lot has scavengers and predators (Jensen, 1987). Al- changed. The kinematics of meiofaunal feeding though some nématodes (as well as meiofaunal has been defined. There are four harpacticoid sized annelids) are deposit feeders, most metazoan feeding groups : point feeders that are sélective meiofauna behavior is adapted to pick spécifie mi- epistrate pickers, line feeders that scrape edges of crobial food items, e.g., microalgae, bacteria, and particles, plane sweepers that sweep food into protozoans. Some workers have referred to this their mouths from two-dimensional surfaces, and feeding habit as «grazing,» and have measured 2 P.A. MONTAGNA how much microbial biomass is consumed by algae (Deco, 1988), and one study used fluores- meiofauna (Montagna, 1984; Decho, 1988; Blan- cence-labeled bacteria to measure grazing on bac- chard, 1991). Whereas macrofaunal (and pre- teria (Epstein and Shiaris, 1992). Both of thèse sumably meiofaunal) deposit feeders have fluorescence techniques are very powerful and adaptations to acquire food by ingesting large have advantages for studies spécifie to bacteria or volumes of sédiment (Lopez and Levinton, 1987), microalgae. The radioisotope approach has prob- meiofaunal grazers have adaptations to pick out lème, but it is currently the only way to measure spécifie microbial particles (Marcotte, 1977 in grazing on both bacteria and microalgae. There- Hicks and Coull, 1983; Jensen, 1987). fore, this review will mostly cover radioisotope One of the most successful areas of study tracer studies. There are two techniques for em- during the 1980's was to measure how much ploying radioactive tracers to measure the inverte- meiofauna eat in the field. It was found that meio- brate feeding via grazing. Microbial food is either fauna can vary their ingestion rates of microbes pre-labeled (Haney, 1971) or labeled while it is in response to changes in food quality or quantity being grazed (Daro, 1978). Both techniques have (Deco, 1988; Montagna and Yoon, 1991). Thèse advantages and disadvantages that limit their use results suggest that meiofaunal grazing rates are to either laboratory or field studies. The pre-label- a functional response to changes in the environ- ing technique requires growing microbes with a ment. I use this term in the same way that Taghon radioactive tracer, introducing the labeled microbe and Green (1990) defined functional response : to the existing microbial community and knowing «how any animal changes its feeding rate in re- the spécifie activity of the food source. Such con- sponse to changes in abundance of its food. » ditions are best achieved in laboratory studies. Meiofauna, particularly harpacticoids, can ex- The synoptic labeling technique is more amenable ponentially increase feeding rates as a function of to in situ studies, because only the radioactive increased microphytobenthos (Montagna, et al, tracer is introduced and microbial uptake of the 1995). More information is needed on how to tracer and meiofaunal grazing can be measured at apply models to meiofauna feeding, but we need the same time. a reliable and easy way to obtain feeding rate It is difficult to review the literature and dé- measurements. The current radioisotope tech- termine the comparative quantitative différences niques are neither well understood, nor easy to in meiofaunal microbivory, because of différences use (Montagna, 1993). in approach to measuring feeding rates and diffé- Together nématodes and harpacticoids usually rences in reporting the rates measured. In large make up 90-98 % of the meiofaunal community part, the différences exist because différent end- (Mclntyre, 1969; Coull and Bell, 1979; Dye and points are desired. Studies on carbon flow might Furstenburg, 1981; Platt, 1981). This paper fo- report rates on a biomass spécifie basis (e.g., |Xg 1 cuses on nématodes and harpacticoids because C • ind • h" ), whereas studies on the impact of they dominate the community. So, when I refer meiofauna grazing on microbial populations might 1 to metazoan meiofauna, I am referring to mainly report the flow rate (e.g., h )- The focus of this nématodes and harpacticoids and exclude benthic review is on assessing the latter issue, therefore microfauna (flagellâtes, ciliates and foraminifera). I have reported flow rates. This requires that the There is no doubt that microfauna are important, amount of food (e.g., carbon, chlorophyll, or num- but they may have différent behavior and meta- ber of cells) offered or available for eating is bolism than metazoan meiofauna (Rivkin and De known and reported. In this case it is simple to Laca, 1990). Meiofauna can utilize organic matter calculate the flow rate, i.e., the percent grazed per in diverse forms, but this review is focusing on unit time. An advantage to reporting the flow rate the utilization of the microflora : bacteria and mi- is that the inverse is the turnover time required crophytobenthos. The main purpose of this paper for the microbial population to maintain itself is to review the current literature on meiofaunal under the grazing pressure of meiofauna. Turnover feeding rates, so that the rôle of meiofauna in time is an interesting number, because if the graz- transferring microbial carbon into food webs can ing rate is near the prey population growth rate be better appreciated. then there is a tight linkage between predator and prey.

TECHNIQUES MEIOFAUNAL GRAZING RATE STUDIES IN THE LABORATORY

Most meiofaunal grazing rate studies have em- ployed radioisotopic tracers. There are two notable The earliest study on nématodes was performed exceptions. One study used chlorophyll-pigment by Duncan et al. (1974). They pre-labelled bac- gut-content analysis to measure grazing on micro- teria, Acinetobacter sp., with 14C-glucose and fed MEIOFAUNAL MICROBIVORY 3 them to a freshwater nematode, Plectus palustris, but the weight spécifie grazing rate decreased in hanging drops on slides. Although the grazing nearly an order of magnitude. One experiment was rate was low (Table I), the amount of bacteria con- performed with the diatom N. salinarum, and the sumed was 650% of the nematode body weight feeding rate was four times higher on this dia- d*1, Another early study on the marine nematode, tom, indicating that sélection of food species Adoncholaimus thalassophygas, demonstrated that exists. this predator could take up dissolved organic mat- Herman and Vranken (1988) fed the nematode 14 ter (DOM) in the form of C-glucose, but did not Monohystera disjuncta with the bacterium Altero- eat pre-labelled bacteria (Lopez et al., 1979). monas haloplanktis in bacto-agar. Feeding rates Admiraal et al. (1983) fed the nematode Eudi- increased with âge, but females had greater feed- plogaster pararmatus l4C-labelled algae, Navicula ing rates than maies (Table I). They also measured pygmaea. They used an interesting technique. The défécation rates and used a model to calculate as- diatoms were solidified in agar and nématodes in- similation efficiency. The assimilation efficiency troduced to the agar drops. This is one of the most was low : 18 % for juvéniles, 27 % for adult maies, complète studies in terms of measuring functional and 26% for adult females. responses, since they used three concentrations of Diatom ingestion rates increase with âge and food, two âges of nématodes, and two species of size for the nematode Chromadorita tenuis (Jen- food. Feeding rates increased with increasing food sen, 1984). The nematode body weight increases concentration. In two of the three experiments, about 20 times during its life cycle, and the in- there appears to be a saturation of the feeding rate. gestion rate increases from about 1 to 3 (Ag algae Feeding rates doubled with doubled nematode âge, d1.

Table I. - Meiofaunal grazing rates using prelabelled food. The grazing rate was calculated as the fraction of radioactivity incorporated per individual. Units are in x 10~4 h"', which is équivalent to% x 100 h1.

Taxa Bacteria Microalgae Référence

Nématodes Plectus palustris 3.2 Duncan et al. (1974) Adonchholaimus thalassophygas 0.016 Lopez et al. (1979) Eudiplogaster pararmatus 0.02 Admiraal et al. (1983) Monohystera disjuncta (Juvénile) 17.8 Herman and Vranken (1988) Monohystera disjuncta (Maie) 15.3 - Herman and Vranken (1988) Monohystera disjuncta (Female) 53.1 Herman and Vranken (1988) Harpacticoids Tisbe californiens 1.6 Lear & Cppenheimer (1962) Tisbe holothuriae 1.2 Vanden Berghe & Bergmans, (1981) Tisbe holothuriae (sand) 19.7 Rieper (1978) Tisbe holothuriae (suspension) 0.059 Rieper (1978) Tisbe battagliai 1.2 Vanden Berghe & Bergmans, (1981) Tisbe furcata 0.51 Vanden Berghe & Bergmans, (1981) Paramphiacella vararensis (sand) 0.059 Rieper (1978) Paramphiacella vararensis (suspension) 0.0049 Rieper (1978) 4 P.A. MONTAGNA

It appears that ail aspects of nematode biology algae and preferred the bacteria, and two had the is strongly influenced by the amount of food same rate and preferred the algae (Table I). How- available. Schiemer (1982) measured respiration, ever, I think that Vanden Berghe and Bergmans growth, and reproduction of Caenorhabditis may have misinterpreted the results. They per- briggsae as a function of différent concentrations formed seven experiments, but the experiments of the bacterium, Escherichia coli. Nematode usually contained différent amounts of added body length and weight increased concordantly algae and bacteria for différent replicates. Within when grown with increasing concentrations of the experiments, there are trends of increasing bacteria. Nematode respiration increased with in- grazing rates with increasing added algae (Fig. 1). creasing food. Growth rates increased with in- Although, T. furcata had an average grazing rate creasing food to a threshold value, and maturation four times lower than the other two species, the was earlier at higher food densities. Fecundity, experiments also contained an average of 40% egg size, and egg production also increased with less food in each replicate. Rather than an in- increasing food. The nematode Plectus palustris trageneric effect, they may have simply observed showed a similar response (Shiemer et al., 1980). a functional response to the amount of added food Both species have increased assimilation, growth, (Fig. 1). and population rate with an increase in bacterial Ontongenetic feeding shifts also occur within food density (Schiemer, 1983). Thèse studies de- the harpacticoids (Decho and Fleeger, 1988). Ni- monstrate the tight linkage between nématodes tocra lacustris feed on diatoms only from the sec- and the amount of bacterial food available. ond or third copepodite stage. Nauplii and early The first study on harpacticoids was performed copepodite stages ingest bacteria by scraping the by labelling the green alga, Platymonas subcordi- outer surface of diatoms. Adults ingest bacteria formis, with 90Sr and 90Y (Lear and Oppenheimer, coincidently with ingested diatoms. 1962). However, they used Tigriopus californicus, Food quality, as measured by C:N ratios, does a harpacticoid that is not benthic. Tigriopus is a not affect ingestion rates of Tisbe cucumariae. littoral tide pool species. Syvitski and Lewis Guidi (1984) fed T. cucumariae seven pre-labelled (1980) studied sédiment ingestion and minerai foods with varying C:N ratios and protein content. transformation by T. californicus. They found that Whereas nitrogen, protein level, and C:N ratios ingestion rate was dépendent on suspension con- significantly correlated with survival and develop- centration. ment times, ingestion rates were not greatly af- Rieper (1978) performed one of the first studies fected. feeding bacteria to harpacticoids. She used a planktonic species, Tisbe holothuriae, and a benthic species, Paramphiascella vararensis. She pre- labelled five différent strains of bacteria with 3 3 H-glucose or H-leucine, and offered the harpac- 2.0 ticoids a sand-paste consisting of pelleted bacteria in sterilized beach sand and bacteria in suspension. We don't know in which experiments glucose or leucine were used, and this could have affected the results. Both species had higher graz- 1.5 ing rates when offered bacteria in a sand paste over bacteria in suspension. Unexpectedly, the planktonic species grazing rate was three orders of magnitude greater on sand than suspension, but £ 1.0 the différence was only one order of magnitude for the benthic species (Table I). This suggests that even planktonic harpacticoids are episubstrate feeders. Rieper obtained three other results : the 0.5 planktonic species ate more than the benthic spe- Tisbe furcata cies, both species had différent rates on différent T. battagliai species of bacteria, and both species had higher T. holothuriae grazing rates when the cell concentration were in- 0.0 creased. 20 40 60 80 100 120 140

Harpacticoids also may have intrageneric Carbon Added (pg) différences in feeding rates and préférences. Three species of the planktonic genus Tisbe were fed Fig. 1. - Functional response of Tisbe spp. to added pre-labelled algae {Dunaliella tertiolecta) and un- food. Data from Vanden Berghe and Bergmans (1981) labelled bacteria (Vanden Berghe and Bergmans, < k c> is fit to exponential model, G=Gmax (l-e ), suggested 1981). One species had a low feeding rate on by Montagna et al. (1995). MEIOFAUNAL MICROBIVORY 5

One measure of food quality is egg production. Bauer, 1988), or adsorb dissolved inorganic carb- The harpacticoid copepod, Heteropsyllus pseudo- on (Montagna, 1983). A properly designed in situ nunni, produced more eggs when fed détritus from meiofaunal grazing experiment must consider and Juncus roemerianus than when fed the microalga, correct for isotopic uptake by microbes, meio- Dunaliella sp. (Ustach, 1982). The copepod also fauna, and macrofauna via non-grazing processes. produced more eggs when fed Juncus détritus and This requires parallel incubations to obtain expéri- bacteria than when fed the microalga Nitzschia sp. mental and control values. (Ustach, 1982). Thèse results suggest that détritus Carman and Thistle (1985) used this technique and the associated bacteria are important to H. to study species interactions and feeding straté- pseudonunni. However, the copepod Scoîtolana gies. They injected 14C-bicarbonate or 14C-acetate canadenensis produced more eggs on a mixed diet into undisturbed sédiment cores and incubated for of algae and bacteria than either diet alone (Heinle 4 and 8 hours. They found that three co-occurring et al, 1977). species had three différent feeding stratégies. Thompsonula hyaenae preferred microalgae, Halicyclops coulli preferred bacteria, and Zau- sodes arenicolus did not exhibit préférences IN SITU GRAZING RATE STUDIES (Table II). In gênerai, the grazing rates from field studies (Table II) are much lower than the grazing Microbial prey can also be labeled while they rates obtained from laboratory studies (Table I). are being grazed (Daro, 1978). I have adapted this This could be explained in two ways. There may be methodological problems with the in situ tech- technique for use in sédiments to measure meio- nique, or the lower rates may be a response to faunal grazing rates (Montagna, 1984; Montagna lower amounts of food. It is more likely that food and Bauer, 1988; Montagna, 1993). This allows is added in excess in laboratory culture experi- for in situ studies to be performed. Meiofaunal grazing rates on bacteria and microalgae are cal- ments than is available in the natural sédiments culated using a model proposed by Daro (1978). during field studies. Therefore, it is possible (and perhaps likely) that the lower grazing rates are re- The meiofaunal grazing rate (G) is the proportion flecting lower amounts of available food. of material flowing from the donor (or prey) compartment to the récipient (or grazer) compartment Recently, Carman (1990) has suggested that per unit time. The model assumes that label is in thèse différences in grazing rates among the three excess and that during the incubation period label species were due to label uptake by epicuticular does not become limiting, prey uptake is linear, bacteria, and not grazing on labeled bacteria. Maie and grazer label recycling is zéro. In this case, G copepods do not feed while clasping females, but is expressed in units of h1 and is calculated as the females continue to feed. No bacteria as- follows : sociated label was seen in copepod guts by auto- radiography, and non-feeding maies still G = 2F/f (1) incorporated label on their cuticle. Carman (1990) concluded that différences in feeding rates on bac- F = M/B (2) teria among the harpacticoids listed in Table II is where F is the fraction of label uptake in the due to différences in uptake by epicuticular bac- grazer, M (in this case meiofauna), relative to the teria, not grazing on labeled bacteria. This study prey, B (bacteria or microalgae), at time, / in illustrâtes the importance of using live controls to hours. M and B are in units of disintegrations per subtract label uptake by non-grazing processes. minute (DPM). Since lit is a constant, variability Most authors have used the in situ technique in G is due to variability in F, i.e., M and B. In to measure carbon flow, and not individual species situ grazing studies require controls, because responses to environmental factors. The goal in meiofauna may absorb DOM (Montagna and thèse types of studies is to détermine the impact

Table II. - Copepoda grazing rates from studies that label food while grazing occurs. Grazing rate was calculated as two times the fraction of radioactivity incorporated per unit time (Daro, 1978). Units are in x 10"4 h"', which is équivalent to % x 100 h ".

Taxa Bacteria Microalgae Référence

Thompsonula hyaenae 0.002 0.056 Carman & Thistle (1985)

Halicyclops coulli 0.016 0.002 Carman & Thistle (1985)

Zausodes arenicolus 0.008 0.007 Carman & Thistle (1985) 6 P.A. MONTAGNA

of meiofauna on benthic microbial productivity, creased primary production within 2-3 weeks, and and the flow of carbon from microbes to meio- this lead to increases in meiofaunal grazing rates. fauna. I have performed five such studies During the four week experiment, bacterial pro- (Table III). duction was not stimulated, and grazing rates on The community grazing rates on bacteria range bacteria did not change. This study shows that only within one order of magnitude, from 0.003 meiofaunal communities can respond to changes to 0.03 h1. The range on microalgae is fives times in the quantity of food abundance with changes greater, i.e. a 50 fold différence, from 0.0008 to in ingestion rates. 0.04. The range on both grazing rates reflects the Only one study has come to the conclusion that range of environmental conditions, e.g., tempéra- meiofauna grazing has no impact on bacterial dy- ture, season, and food quality. In my studies, the namics (Epstein and Shiaris, 1992). They con- différences can be explained by température and cluded that meiofauna consumption only organic carbon content of the sédiment (Montagna accounted for about 0.03 % of the bacterial stand- and Yoon, 1991). In each study, différent taxa ing stock per day. This is équivalent to a meio- dominate the grazing process, reflecting différ- faunal grazing rate of 0.0000125 h"1, which is ences in community structure in each locale and about three orders of magnitude lower than ail experiment. The average grazing rate over ail stu- other estimâtes reported in the literature dies is the same for both bacteria and microalgae : (Table III). In fact, the estimate is comparable to 0.01 h1. This suggests, that on average the meio- rates of individual organisms, and not communi- faunal community is removing 1 % of the (heter- ties (Tables I and II). This resuit is at odds with otrophic and autotrophic) microbial standing stock most published literature. The différence must be per hour Worldwide (in shallow ecosystems). attributed to one or more unique circumstances, The mesocosm study by Nilsson et al. (1991) e.g., the use of a différent technique, the spécifie was the only expérimental study. They were in- location, or the bacteria used. The technique, vestigating the effect of increased nitrogen (N) fluorescence-labeled bacteria, appears to be a very and phosphorous (P) loading on the lower trophic powerful method. However, rather than staining a levels of a sand System. Additions of N and P in- broad natural community, four strains of coliform

Table III. - Meiofaunal community grazing rates from studies that label food while grazing occurs. Grazing rate was calculated as two times the fraction of radioactivity incorporated per unit time (Daro, 1978). Units are in h"1, which is équivalent to % x 100 h"1.

Habitat Location Bacteria Microalgae Référence

Sait marsh North Inlet, SC 0. .0337 0. .0065 Montagna i ;i984)

Beach San Francisco Bay, CA 0. .0028 0. .0008 Montagna 5i Bauer (1988)

Subtidal San Antonio Bay, TX 0, .0099 0. ,0411 Montagna s , Yoon (1991)

Océan 18m Santa Barbara, CA 0. .0058 0. ,0018 Montagna et al. (1994)

Oyster pond La Rochelle, France - 0.,007 0 Blanchard (1991)

Mesocosm Tjârnô, Sweden 0. .003 0.,00 4 Nilsson et : al. (1991)

Mud flat Ems-Dollard, - 0,,00 3a Admiraal s ;t al. (1983)

Netherlands

Mud flat Marennes-Oléron Bay, 0.0014 Montagna et al. (1995)

France

Mud flat Boston Harbor, MA 0.00001b Epstein & Shiaris

(1992)

aDifferent technique: estimate based on laboratory cultures bDifferent technique: estimate based on fluorescence-labeled- bacteria MEIOFAUNAL MICROBIVORY 7

bacteria were used, two extracted from sewage ences also exist. Intrageneric grazing rates may treatment plant effluent. The natural community exist, but more work is needed on this issue. It was reported to be dominated by rod-shaped bac- is possible that most bacteria ingested by meio- teria. There are one of two possibilities that must fauna in shallow water, is coincidental ingestion. be explored in future research : technology and There is much variability from site to site World- spatial variability. Perhaps grazing rate results are wide, because of differing amounts of food avail- a function of the technique used and one technique able due to différent environmental conditions and (or the application of it) may be flawed. Alterna- meiofauna community structure différences. tively, grazing rate results are always unique to Despite this variability, grazing rates only vary by the study area and not gênerai (in this case Boston an order of magnitude, and on average meiofauna Harbor just represents the low end of the spec- graze at a rate of 0.01 • h1, or 1 % of the standing trum). In either case, much more work is needed. stock of both heterotrophic bacteria and auto- Results from freshwater studies are in the same trophic microalgae. As long as the average global ranges as those found in marine studies. Attheyella microbial turnover time is about 4 days or less, sp. in freshwater streams ingest bacterial carbon meiofauna grazing will be roughly in equilibrium at rates of 0.03-0.47 (Xg • ind"1 • d1 (Perlmutter with microbial production. This suggests that and Meyer, 1991). This is comparable to rates of meiofaunal communities are tightly coupled to mi- 0.05-0.12 (xg • ind1 ■ d1 that is reported for Tisbe crobial communities. This coupling implies that sp. (Vanden Berghe and Bergmans, 1981). The meiofauna have a significant global impact on mi- total stream community is grazing bacteria at rates crobially mediated processes by allowing micro- that range from 0.0004 to 0.0092 h1, which is in bial growth rates to be maintained in log phase. the low range for marine meiofauna (Table III). ACKNOWLDGEMENTS - I am grateful to the anony- The lower rates are concordant with the densities mous reviewers who gave me many helpful sug- of meiofauna in streams, which is about an order gestions. This is University of Texas Marine of magnitude lower than in marine sédiments. The Science Institue Contribution number 919. comparability of thèse rates indicate that the conclusions drawn from marine habitats have gener- ality to ail aquatic habitats that support meiofauna communities. REFERENCES Metazoan meiofauna are not the only grazers in the benthos (Lee et al., 1966). Protozoans are also important in some environments (Fenchel, ADMIRAAL W., L.A. BOUWMAN, L. HOEKSTRA 1977 ; Epstein and Shiraris, 1992), but perhaps not and K. ROMEYN, 1983. Qualitative and quantitative others (Kemp, 1988). Temporary meiofauna, and interactions between microphytobenthos and her- taxa other than harpacticoids and nématodes can bivorous meiofauna on a brackish intertidal mudflat. also be important grazers. For example, poly- Int. Revue ges. Hydrobiol. 68 : 175-191. chaetes (Montagna, 1984), mollusks (Montagna BLANCHARD G.F., 1991. 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différent densities of bacterial food and gênerai eco- USTACH J.F., 1982. Algae, bacteria and détritus as logical considérations. Oecologia 44 : 205-212. food for the harpacticoid copepod, Heteropsyllus SYVITSKI J.P. and A.G. LEWIS, 1980. Sédiment in- pseudonunni Coull and Palmer. J. Exp. Mar. Biol. jestion by Tigriopus californicus and other zooplank- Ecol. 64 : 203-214. ton : minerai transformation and sedimentological VANDEN BERGHE W. and M. BERGMANS, 1981. considérations. J. Sed. Petrol. 50 : 869-880. Differential food préférences in three co-occurring TAGHON G.L. and R.R. GREENE, 1990. Effects of species of Tisbe (Copepoda, Harpacticoida). Mar. sediment-protein concentration on feeding and Ecol. Prog. Ser. 4 : 213-219. growth rates of Abarenicola pacifica Healy et Wells (Polychaeta : Arenicolidae). J. Exp. Mar. Biol. Ecol. Reçu le 5 septembre 1994 ; received September 5, 1994 136 : 197-216. Accepté le 28 septembre 1994; accepted September 28, 1994