Microb Ecol (1994) 28:195-199

Sources of Carbon for the Microbial Loop

MICROBIAL ECOLOGY © 1994Springer-VerlagNew York Inc.

The Microbial Loop in Flowing Waters J.L. Meyer Institute of Ecology, University of Georgia, Athens, Georgia 30602-2602, USA

Abstract. The microbial loop in flowing waters is dependent on allochthonous sources of carbon, which vary in quality. The proportion of dissolved organic carbon (DOC) that can be degraded ranges from < 1 to over 50%, and the bioavailability of DOC (micrograms bacterial biomass produced per milligram DOC present) ranges over two orders of magnitude. Bioavailability of DOC is predictable from the ratio of H/C and O/C of the DOC, but further work is needed to develop simple predictors of bioavailability of DOC in a range of environments. Consumers of bacteria in streams range in size from protists to insect larvae, with highest rates of bacterial consumption found among the meiofauna and certain filter feeders and grazers. Because there appear to be fewer trophic transfers in the lotic microbial loop, it functions more as a link in flowing waters than it appears to do in the marine plankton. Ecologists have long been aware of the importance of detrital food webs in lotic ecosystems. In the same year and journal in which Pomeroy's seminal paper on the marine microbial loop was published, Cummins [4] diagrammed the food web of a headwater stream in which bacteria and fungi were recognized as decomposers, as a nutritional resource for insect consumers of decaying leaves, as consumers of dissolved organic matter, and as part of a pool of fine particulate organic matter that was consumed by insect larvae. Although the microbial loop was not yet named, it is clear that lotic ecologists recognized the trophic significance of bacteria. The objective of this paper is to briefly consider sources of carbon for and consumers of the microbial loop in flowing waters. In well-lit streams, autochthonous sources of organic carbon are significant; in shaded streams, most of the carbon comes from the catchment or floodplain, and there is little coupling between algae and bacteria [3]. Overall, flowing waters are more dependent on allochthonous sources of both carbon and bacteria [12] than are other ecosystems. Hydrologic flow path in the catchment and residence time of water in soil horizons that differ in organic matter content and sorption capacities control the amount and character of dissolved organic carbon (DOC) entering streams. Particulate organic matter (e.g., leaf litter) is an important carbon source for the microbial loop. Leaf litter serves both as a substrate for bacterial and fungal growth and a source of DOC. In addition to an initial pulse of rapidly leachable, watersoluble material from freshly-fallen leaves, there is a slow release of DOC from

196

J.L. Meyer

Table 1. Bioavailability of DOC expressed as the ability of bacteria to grow on DOC from different sources. Bioavailability was assessed during short-term (3-4 day) bioassay experiments in which native bacteria were enriched with DOC from different sources, and the accumulation of bacterial biomass was measured in laboratory incubations without predators. Values reported are measured amount of bacterial carbon accumulated per unit of DOC present. Ecosystem Humic fractions Blackwater swamp Reservoir Suwanee River

tzg Bacterial C per mg DOC

Ref.

0.7-2.9 14-40 17a

15 15 11

20a

11

Water oak

30

14

Willow Cypress Hardwood

7b 17 41

14 c c

59 182

c 10

Nordic humics Leachates

Macrophyte Alligatorweed

Ecosystem Whole water Blackwater swamp Ogeechee River Ogeechee tributaries (high discharge) Hugh White Creek Ogeechee River (high discharge) Ogeechee tributaries (low discharge) Clear lake Humic lake Ogeechee River (low discharge) Reservoir

Ixg Bacterial C per mg DOC

Ref.

1.3-4 2.4-18.4 10--40a

15 11

14.5b 20-70Q

14 11

20-70~

11

30-44 32-35 50-100a

20 20 11

44-68

15

a Corrected values; wrong biomass conversion factor used in original paper bLow estimate because of flagellate grazing during experiment. cj. Meyer and J. Weis, unpublished data, University of Georgia (see [19]).

organic matter stored in the stream bed. This release can be accelerated by feeding activities o f invertebrates [ 13]. The extent to which sources of D O C for the stream are the same as sources o f carbon for the microbial loop depends on the degree to which D O C is refractory. The proportion of D O C that can be degraded is highly variable, ranging from < 1% for humic and high molecular weight fractions o f D O C [ 14, 15] to over 50% for low molecular weight [14] or anthropogenic D O C [18]. Solar radiation can alter this degradability: labile D O C is formed from refractory D O C in the presence o f sunlight [5]. Because o f this variation in D O C quality, the amount o f D O C entering the system is not a measure o f D O C supporting the microbial loop. One measure o f that is the amount o f bacterial biomass produced per unit D O C present, which has been determined using bioassays (Table 1). This does not include the amount o f D O C used by bacteria in respiration, because that carbon is not available to higher consumers. Bioavailability of D O C ranges over two orders o f magnitude (Table 1). This wide range in bioavailability points to the need for an indicator of D O C quality that does not require an analysis o f all constituent organic compounds. Development o f a simple measure o f D O C quality is needed to stimulate progress in understanding carbon sources for freshwater and marine microbial loops. Both ultrafiltration and resins have been used to partition D O C into fractions of different lability [14, 15]. Current research suggests that simple measures o f elemental

Lotic Microbial Loops

197

60

-6"

50

~g ~

=

3o-

~

-~ ;.Z

20-

~o-

Y joe

o

•

,

10

.

,

,

2o

30

.

,

,

40

50

Observed bioavailability (pg bacterial C/mg DOC)

,

, 60

Fig. 1. Atomic ratios of H/C and O/C in DOC were used to predict bioavailability of DOC to bacteria (txg bacterial C produced per mg DOC present) with the following equation: bioavailability = 39.08 H/C - 49.16 O/C (r2 = 0.93, P < 0.001). Predicted bioavailability is compared with observed bioavailability (3-day laboratory growth experiments). The line indicates a 1:1 relationship.

composition of DOC offers considerable promise as an indicator of quality. As part of a collaborative project with E.M. Perdue (Georgia Institute of Technology, Atlanta, Georgia), we have determined bacterial growth on DOC [11 ] concentrated from plant leachates and river water with reverse osmosis [17], followed by cation, silica, and sulfuric acid removal and freeze drying [19]. Atomic ratios of H/C, N/C, and O/C can be calculated after CHN analysis and ashing of freeze-dried DOC [19]. Availability of DOC to bacteria (micrograms bacterial C per milligram DOC present) can be predicted remarkably well (Fig. 1) with the following equation determined using stepwise linear regression: Bioavailability (txg bacterial C/mg DOC present) = 39.08 H/C - 49.16 O/C (r 2 = 0.93, P < 0.001). Adding N/C to the regression does not improve the fit. H/C is directly proportional to aliphatic content and inversely proportional to aromatic content of DOC [ 19]. Further development of simple measures that predict the ability of bacteria to grow on DOC is a fruitful direction for research. Consumers of bacterial C complete the microbial loop. Those consumers in flowing waters range from flagellates to insect larvae that differ in size and ability to use bacterial C (Table 2). Although bacteria are not a major part of the diet of insects that feed on leaf litter, small protists are significant consumers of bacteria in rivers and streams [ 1, 2]. Aquatic insect larvae are both predators and competitors of microbes: insects consume bacteria and fungi, but they can also digest the detritus that is a bacterial food resource [12]. The true bacterial specialists in flowing waters are meiofaunal organisms, filter feeders, and biofilm grazers: their assimilation of bacterial C (micrograms bacterial C per milligram animal) is 1-4 orders of magnitude higher than any of the other bacterial consumers (Table 2). Therefore, the link between bacteria and large consumers is quite direct in flowing waters. Carbon can move from bacteria to insect consumers in a single trophic transfer. The following key features distinguish riverine and marine microbial loops (Fig. 2): 1. Allochthonous sources of carbon and bacteria are more important in flowing waters. 2. The linkage between benthic and planktonic microbial loops is greater than in many marine environments.

198

J.L. Meyer

Table 2.

Assimilation of bacterial C by consumers in streams measured using radiolabeled bacteria. Fg Bacterial C per mg animal per day

Organism Stoneflies (Peltoperlidae) Craneflies (Tipula) Isopods (Lirceus) Ciliates Flagellates Harpacticoid copepod (Atthyella sp.) Mayflies (Stenonema sp.) Black flies (Simulium spp.)

Floodplain and Catchment ~"

I',I

Matter

'

~"

'

" "/

/

+ ¢ Invertebrate [~11' and rVertebrate Predators

Light

ooc ',/

~1[ Shredders | / Meiofauna k l [ I 1

I

Groundwater Soil water

9 9 8 2 2 16 7 6

~.- ~_~---Refractory.~_.Labile I

Particulate Coarse Organic

i

1-2 x 10 -4 5 X 10 - 4 0.7-6 X 10 - 3 6 x 10 _2 2.8 x 10 -1 1-36 2 16-267

Reference

I~ I I

'5'

,oi

t~

Alga'-~

I

I I

I

I = age a,ee

l ' . , I,Me'°tau".a 1 ~copepoos, lJ'~ nematodes,

L

I ~

I Ciliates

~ i It°tilers}

t

~(

/ / -4

!

t , / ~1 I ~' I " CO ector-filterers (e g b ack f y) Collector-gatherers (e.g. midge) Scrapers (e.g. mayf y)

|

Fig. 2. Simplified diagram of a lotic food web showing sources and major pathways of organic carbon. Dotted lines indicate flows that are a part of the microbial loop in flowing water but not in planktonic systems.

3. Both bacteria and fungi are associated with large particles and hence are directly available to larger-sized organisms in streams. 4. Because macroscopic consumers that feed directly on bacteria are abundant, there are fewer trophic transfers between bacteria and top consumers, and hence the microbial loop functions more as a link in flowing waters than it does in planktonic ecosystems [12]. Acknowledgements. This research has been supported by National Science Foundation grants BSR 8705744 and 9011661. Thanks to Mary Ann Moran, Bob Hodson, and Bill Wiebe for organizing this symposium in honor of Larry Pomeroy, whose research has inspired much of my work. He has been a valued colleague for many years. References

1. Bott TL, Kaplan LA (1990) Potential for protozoan grazing of bacteria in streambed sediments. J N Am Benthol Soc 9:336-345

Lotic Microbial Loops

199

2. Carlough LA, Meyer JL (1991) Bacterivory by sestonic protists in a southeastern blackwater river. Limnol Oceanogr 36:873-883 3. Couch CA, Meyer JL (1992) Development and composition of the epixylic biofilm in a blackwater river. Freshwater Bio127:43-51 4. Cummins KW (1974) Structure and function of stream ecosystems. BioSci 24:631-641 5. DeHaan H (1993) Solar UV-light penetration and photodegradation of humic substances in peaty lake water. Limnol Oceanogr 38:1072-1076 6. Edwards RT, Meyer JL (1987) Bacteria as a food source for black fly larvae in a blackwater river. J N Am Benthol Soc 6:241-250 7. Edwards RT, Meyer JL (1990) Bacterivory by deposit-feeding mayfly larvae (Stenonema spp.). Freshwater Biol 24:453-462 8. Findlay S, Meyer JL, Smith PJ (1984) Significance of bacterial biomass in the nutrition of a freshwater isopod (Lirceus sp.). Oecologia 63:38-42 9. Findlay S, Meyer JL, Smith PJ (1986) Incorporation of microbial biomass by Peltoperla sp. (Plecoptera) and Tipula sp. (Diptera). J N Am Benthol Soc 5:306-310 10. Findlay S, Carlough L, Crocker MT, Gill HK, Meyer JL, Smith PJ (1986) Bacterial growth on macrophyte leachate and fate of bacterial production. Limnol Oceanogr 31:1335-1341 11. Left LG, Meyer JL (1991) Biological availability of dissolved organic carbon along the Ogeechee River. Limnol Oceanogr 36:315-323 12. Meyer JL (1990) A blackwater perspective on riverine ecosystems. BioSci 40:643-651 13. Meyer JL, O'Hop J (1983) Leaf-shredding insects as a source of dissolved organic carbon in headwater streams. Am Midl Nat 109:175-183 14. Meyer JL, Edwards RT, Risley R (1987) Bacterial growth on dissolved organic carbon from a blackwater river. Microb Ecol 13:13-29 15. Moran MA, Hodson RE (1990) Bacterial production on humic and nonhumic components of dissolved organic carbon. Limnol Oceanogr 35:1744-1756 16. Perlmutter DG, Meyer JL (1991) The impact of a stream-dwelling harpacticoid copepod upon detritally-associated bacteria. Ecol 72:2170-2180 17. Serkiz SM, Perdue EM (1990) Isolation of dissolved organic matter from the Suwannee River using reverse osmosis. Water Res 24:911-916 18. Servais P, Gamier J (1993) Contribution of heterotrophic bacterial production to the carbon budget of the River Seine (France). Microb Ecol 25:19-33 19. Sun L (1993) Isolation, characterization, and bioavailability of dissoved organic matter in natural waters. Ph.D. Dissertation. Georgia Institute of Technology, Atlanta. 20. Tranvik LJ, Hofle MG (1987) Bacterial growth in mixed cultures on dissolved organic carbon from humic and clear waters. Appl Environ Microbiol 53:482-488