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THE ROLE OF LCARVAL CHIRONOMIDAE IN THE PRODUCTION OF LACUSTRINE COPROPEL IN MUD LAKE, MARION COUNTY, FlLORIDAl A. J. Iovino Department of Zoology, Indiana University, Bloomington 47401 and W. H. Bradley U.S. Geological Survey, Washington, D.C. ABSTRACT Mud Lake is a shallow (avg 45 cm), alkaline (pH 7.7-10.2), brown-water lake having an area of about 180 ha. A study of its organic sediment was undertaken because it appears to be a present-day analoguc of the richly organic lacustrine oozes that were the precursors of the oil shales of the Green River Formation (Eocene). The water contains about 200 ppm total dissolved solids. The soft ooze is about 1 m thick and consists of minute fecal pellets produced primarily by larvae of Chironomus (Chironomus) sp. Mean numbers of larvae ranged from 120 to 580 m-‘; such a small population may reflect extensive predation by fish. The small diversity of Chironomidae at this latitude may reflect the fact that few organisms can tolerate the physical conditions produced by the shallow water. Experiments with laboratory-reared Mud Lake midges showed that the numbers of fecal pellets produced generally increased with the concentration of algal cells available; that only when the larvae were fed blue-green algae were the fecal pellets coherent and durable-larvae fed green algae produced pellets that disintegrated, returning the undigested algae to the food supply; and that larvae fed blue-green algae changed from filter-feeding to grazing on the fecal pellets when suspended algal cells bccamc sparse. We conclude that the sediment in Mud Lake is pclletal because only blue-green algae are available fol food and that the larvae probably graze because all the blue-greens live only on, or in, the fecal pellets. Early instars produce ovoid pellets; later instnrs produce longer, cylindrical pellets. The analogy between the Mud Lake pelletal ooze and the Eocene precursors of the Green River Formation oil shale is enhanced by the facts that some oil shale thin sections show minute fecal Dellets and that certain beds of rich oil shale contain numerous unmincralized remains of- immature chironomids. INTRODUCTION During the first quarter of this century one of us (W. H. B.) began a search for a modern analogue of the lacustrine organic ooze thought to have been the precursor of the rich oil shale beds so numerous in the Green River Formation (Eocene) of Wyoming, Colorado, and Utah. It was not until a few years ago that several such analogues were found ( Bradley 1966). Among these, the algal sediment forming in Pilkington Bay at the north end of Lake Victoria was most instructive because Beauchamp’s (1964) studies showed that, in its l Yublication authorized Geological Survey. by the Director, natural environment, it was virtually immune to bacterial decay and hence was an energy sink. Our study deals with a comparable algal sediment now being formed in Mud Lake, Florida. MUD LAKE ENVIRONMENT AND SEDIMENTS Mud Lake is in the Ocala National Forest remote from the influence of any human activity. The lake occupies an ancient sink hole, is roughly elliptical, and has an area of about 180 ha. Its depth averages about 45 cm, changing from about 22 cm in the driest seasons to about 85 cm during the wettest. Through the greater part of the year ( March through November ) , water U.S. temperature ranges from 21.3 to 30.7C and 898 LACUSTRINE COPROPEL averages 26.7C. During the short winter ( December through February), water temperature ranges from 6.8 to 19.9C and averages KOC. Water color ranges from very pale amber ( virtually colorless) to amber, and the pH ranges from 7.7 to 10.2. Total dissolved solids amount to about 200 ppm, though they vary moderately with lake level. The dominant cations in order of abundance are Ca, Na, and Mg; the dominant anions arc SO4, HCOs, and Cl. The bottom is virtually level, shoaling imperceptibly toward the lake margins, which arc dcfincd by a nearly continuous floating mat of vegetation, dominated now by Eichhornia crassipes and a few years ago by Pistia sp. Back of the floating vegetation, the wet level ground supports a mixed hardwood swamp flora. The extremely soft, fluid, copropelic (Swain and Prokopovich 1954) sediment of Mud Lake is entirely autochthonous. It consists overwhelmingly of blue-green algae or their partly digested remains. Mixed with these are diatom frustules and megascleres of a freshwater sponge. The siliceous particles make up 10 to 15% by weight of the air-dried sediment. All elastic particles of clay, silt, or sand are effectively screened out by the marginal vegetation, Microscopic examination, however, reveals an occasional small grain of quartz sand, which must have been blown in by the wind along with a small amount of pine pollen from the higher land beyond the wet forest belt. This algal ooze forms a layer about 1 m thick. According to l*C determinations by the U.S. Geological Survey, this kind of sediment has been accumulating about 3,000 yr. Below the algal ooze is at least 8 m of saw grass peat. The approximation of 3,000 yr is an interpolation between two dates in the algal ooze layer-one at 0.6 m below the top, 2,540 -t- 200 yr ( W-1978 ) , and one date of 4,100 2 250 yr ( W-1682)) which was obtained from the upper part of the saw grass peat section 0.2 m below the base of the algal ooze layer. The most conspicuous feature of this organic sediment is that it consists wholly of minute fecal pellets (Fig. 1), produced almost solely by chironomid larvae, Indeed, IN MUD FIG. 1. bluogrccn LAKE Fecal pellets made up almost wholly algal cells ( x70). 899 of the majority of these pellets are contained in the chironomid tubes. By far the most abundant midge is Chironomus ( Chironomus) sp., an apparently heretofore undescribed species. The chironomids Procladius ( Psilotanypus) bellus Loew, Procladius culiciformis ( Linnaeus ) , and Tanytarsus (Tanytarsus) sp. also occur, though sparingly. Mud Lake, aside from an erratic winter bloom of Spirogyra and Sirogonium, has virtually no phytoplankton or zooplankton, perhaps owing to the lethal effect of sunlight and predation in the shallow water, which is in continual circulation (Bradley and Beard 1969). The blue-green algae live exclusively in, and on, the fecal pellets, and the diatoms live mostly bctwcen the pellets. This environment is for the most part sheltered from the sun. Although the lake has a large and varied fish fauna, the benthos, apart from the midge larvae, is sparse. It includes one species of minute snail, small populations of copepods, cladocerans, ostracods, and one sponge. Protozoa and rotifers are more common, though far from abundant. Nematodes are present but very rare. Some of these animals venture 900 A. J. IOVINO AND W. I-1. BRADLEY TABLE support 1. Composition of the medium used to the algae ;Fed to the midge Zawae during count&g texts of fecal ejecta Constituent CaCL coc12 FeCL 61120 611,O l l MgSOa MnCh 4H,O NaHC03 NaH2P04 Na2HP04 KNOS NaaMoOd NapEDTA ZnCla l FIG. 2. Mean number of larvae me2 ( solid line) ; vertical bars represent the standard errors of the means. Dashed line indicates the corresponding ratios of second to fourth instars. Data based on a minimum of 20 dredge samples per sampling date. upward from the pelletal ooze but are rarely caught in a plankton net. The blue-green algae are represented by a complex and varied assemblage with Schixothrix, Coccochloris, and Anacystis predominating. Seasonally Spirulina is also abundant. CHIRONOMID POPULATION The midge fauna was sampled first (September 1967) with a small Ekman dredge, which was difficult to hold each time at the same level with respect to the mud-water interface owing to the fluidity of the ooze. But this experience, plus examination of scores of other samples taken for a variety of different studies, demonstrated that the midges occurred predominantly in the upper few centimeters of the ooze. Consequently, a collecting chamber more suitable for use in fluid sediment was designed and built. The effective density of the apparatus was reduced by cementing porous material to a supporting ring so that it floats on the upper surface of the ooze. The collecting chamber (15 X 15 cm) then penetrates the ooze just 2.5 cm. A pair of spring-actuated gates in the bottom of the collecting cell are tripped by a falling weight, and a sample of known area and depth is taken at each station. Figure 2 shows the mean number of mg liter-l 30.0 4.0 194.0 7.5 82.0 8.0 2.5 2.0 0.7 8.0 1,500.o 10.0 midges found in the ooze on the dates indicated, as well as the ratios of second to fourth instars. On each sampling date a minimum of 20 samples was taken distributed at approximately equal intervals along a north-south diagonal of the lake. As can be readily seen by the small standard error of the mean, the midge population was fairly evenly distributed in space. The ontogenetic character of the fauna changed seasonally as evidenced by instar ratios. During September the numbers of second and fourth instars are about equal, but in February and April the fauna is progrcssively dominated by fourth instars pending early spring emergence (see Fig. 2). With the onset of faJ1, the numbers of second instars approximate those of the fourth. Apparently the:re may be several generations of Chironomus sp. in Mud Lake annually. The differences in absolute numbers of larvae between the two September sampling periods may be attributed to the fact that larval numbers are dependent on weather conditions during the adult swarming period. Indeed, abnormally low temperatures characterized the period of decline of the fourth instars. Such effects of weather have been noted by Jonasson ( 1961). Compared with that of many North Temperate Zone lakes, the midge population of Mud Lake is remarkably small. It may be kept low by the predation of the many bottom-feeding fish, as well as top-feeding cyprinodontiforms, which are common. LACUSTRINE COPROPEL IN MUD LAKE 901 Algae used as food sources included the pyrenoidosa and green algae Chlorella Coccomyxa peltigerae and the blue-green Gloeocapsa alpicola. ( Cultures kindly pro700 vided by R. C. Starr, Indiana University.) Their comparable size and shape ensured i ISO Fi equal obtainability as food by the chirono:::: 160 LL mids. For purposes of comparison, all algal k 14” concentrations were expressed in Chlorella 2 p 120 units, based on the mean computed volumes 2 of 200 individuals of each species; concen9 100 $ trations of 10 to 100,000 Chlorella units per 2 60 ml were tested. At least 10 different larvae 60 were run through the successive series of food concentrations for 60 min each and 4” their cjecta counted at IO-min intervals, so 70 that for each food concentration the numbers arc means of at least 10 counts (Figs. 30 40 50 6o 3-5). FIG. 3. Cumulative numbers of fecal ejccta proFecal ejecta production rates of larvae for fed Coccomyxa were as anticipated duced by feeding chironomid larvae the green alga Coccomyxa pe2tigerae in increasing concentrations, continuously feeding larvae: The number which are given on each curve in ChZoreZZa units of ejecta produced increased with increased ml-l. food concentration ( Fig. 3). But this was not so for the larvae fed Chlorella (Fig. 4). PRODUCTION RATES OF FECAL EJECTA At low concentrations ( 1,000 units and less) the number of ejecta produced by larvae Because the highly organic ooze of Mud Lake consists wholly of fecal pellets, it is were comparable with the numbers prodesirable to know if the present midge population could possibly account for them 60 all. Nothing was known about the rates at which they produce fecal ejecta so we conducted the following laboratory inves5o tigations, showing that the rate at which chironomid larvae eject feces depends on c the kinds of algae they feed on and the a 40 concentration of algal cells per unit volume. ;a ; Only blue-green algae give rise to well$ 30 formed and coherent fecal pellets. Egg masses of adult females captured at z 3 2. night were reared in fingerbowls at 25C. An inorganic medium (Table 1) that has 2 proved adequate in the past for growing 10 algae was used, the trace elements being mixed separately and added 5 drops/liter. Fourth instar larvae were held at the 20 10 experimental temperature (2%) in algalfret medium for 1 hr to ensure acclimation FIG. 4. Cumulative numbers of fecal ejecta proand the voiding of gut contents. This culduced by feeding chironomid larvae the green alga ture fluid was then poured off and 300 ml ChZoreZZa pyrenoidosa in increasing concentrations, of the same medium containing a known which arc given on each curve in numbers of concentration of algal cells added. ChZoreZZa cells ml-l. 0 0 10 20 MINUTES 0 902 A. J. IOVINO AND numbers of fecal ejecta proFIG. 5. Cumulative duced by feeding chironomid larvae the blue-green alga GZoeocapsu a&cola in increasing concentrations, which arc given on each curve in Ch2oreZZa units ml-l, duccd at equivalent concentrations of Coccomyxa. With conccntra tions greater than 1,000 units, however, the rate of production after 20 min declined perceptibly at 5,000 units, more markedly at 10,000 units, and conspicuously at 30,000 units. This diminution is shown even better in Fig. 6 where the numbers of ejccta are plotted against the concentration of Chlorella units ( = cells for C72lorella). Larvae fed Gloeocapsa produced fewer ejecta overall (Fig. 5). Cumulative numbers of cjecta produced at concentrations of 10 to 10,000 units were barely greater than numbers produced at the lowest concentrations of either Chlorella or Coccomyxa. At the greatest concentrations of Gloeocapsa ( 100,000 units), the rate of production was high for the first 20 min and thereafter fell off progressively. NUMBERS AND FORM OF FECAL EJECTA The ejecta produced by larvae fed on Gloeocapsa differed in a most striking way from those fed on the two green algae. Ejecta from the Gloeocapsu-fed larvae were well-formed, coherent pellets that accumulated in the culture dishes and were ultimately incorporated into the larval tube. Larvae feeding on the green algae, in contrast, produced ejecta that were unconsolidated so that they disaggregated and the constituent particles recirculated into W. II. BRADLEY FIG. 6,. Numbers of fecal ejecta plotted against the cell concentrations (log scale) of the three species of algae used as food for chironomid larvae. the medium. The important thing about this observation is that in Mud Lake only blue-green algae are available as food for the chironomids, and the midge feces have the form of strongly coherent pellets that are incorporated into their tubes. The marked decrease in the rates of production of fecal ejecta by larvae fed on increasingly large concentrations of Chlorella cells suggests that the inhibitor chlorellin ( Pratt et al. 1944) might be involved. Ryther { 1954) found that Daphnia magna fed senescent cultures of Chlorellu showed much greater inhibition in growth and reproduction than did those fed algae that were in the log-phase of growth. We used only young cultures of algae. However, Pratt ( 1942, 1943, 1944) and Pratt, Oneto, and Pratt (1945) showed that a considerable concentration of the substance accumulated in the inorganic culture mcdium within a few hours after inoculation with Chlorella. Thus, we see no reason to assume that: the inhibitory substance chlorellin should not be effective in young cultures; the fact that Ryther (1954) did not note inhibition in Daphnia cultures fed log-phase algae is not understandable in the light of the earlier work. FEEDING HABIT When the chironomid Gloeocapsa, a surprising OF LARVAE larvae were fed change in their LACUSTRINE COPROPEL IN MUD LAKE 903 This is significant to an understanding of the midge environment in Mud Lake. As already mentioned, aside from a singlo, and . rather erratic, bloom of Spirogyra and no Siroggnium., Mud Lake has virtually All the algae live in, on, phytoplankton. or between the fecal pcllcts. Moreover, this . algal flora consists overwhelmingly of bluc. . greens. It seems to follow, therefore, that . . INSTAR IV the blue-greens that live on, and in, the fecal pellets provide a forage base for the chironomids of Mud Lake. Microscopic examination of a great many fecal pellets collected from the lake bottom convinced us that living blue-greens multiply and prosper on the pellets as a substratum. It is highly probable that some unknown pcrcentage oE these viable algae went through the guts of chironomid larvae; both bluegreen and green algae are known to survive passage through the intestinal tracts of certain fish ( Fish 1955; IIickling 1961)) of migratory waterfowl (Proctor 1959)) and of earthworms (Latimer and Anderson 1965). Our experiments with Gloeocapsa indiI I I I cate that production of fecal pellets by 0.10 0.14 0.18 0 22 larvae that forage, or graze, is a less cfficicnt DIAMETER.mm process than production based on filterFIG. 7. Size differences between fecal pellets feeding of algal cells suspended in the of second and fourth instar larvae of Chironomus water. (Chironomus) sp. Dimensions, in mm, of the fecal In general, early instar larvae of Chironopellets are: Instar II, diameter-range 0.102-0.222, rnus sp. produce pellets that are more nearly mean 0.174; length-range 0.123-0.218, mean 0.168. Instar IV, diameter-range 0.094-0.237, spherical or ellipsoidal, whereas later instars mean 0.165; length-range 0.278-0.374, mean produce more nearly cylindrical and longer 0.342. pellets. The overall result is an ooze that consists of roughly equal numbers of ellipfeeding habit was observed-a change from soidal and cylindrical fecal pellets. filter-feeding to grazing, or foraging. FilterThese fecal pellets differ not only in feeding was a normal way for the larvae shape between instars but also in size, those to harvest algal cells dispersed in the culture of the later instars being larger. More than medium. But, when fed these blue-green 100 each of second instar and fourth instar algae, their fecal ejccta formed coherent larval fecal pellets were measured. All these pellets that retained both viable and partly pellets were produced in the laboratory digested algal cells. Accordingly, dispersed during the feeding experiments with blueGZoeocapsa cells decreased in number as green algae. Only the diameter and length feeding continued and, as a consequence, of each pcllct were measured. The average fecal pellet production also dccreascd, espc- diameter of second instar pellets is nearly cially for the higher concentrations of algal identical with the average diameter of cells (Fig, 5). When dispersed algal cells fourth instar pellets. However, the average became sparse, the larvae changed from length of second instar pellets is only filter-feeding to foraging, or grazing, on the slightly greater than the diameter, whereas live algae in, and on, the fecal pellets. the length of fourth instar pcllcts is more 904 A. J. IOVINO AND W. II. BRADLEY FIG. 8. Photomicrograph of fossil, but unmineralized, remains of the labial plate of a midge larva having orthocladiine (incl. Diamesini) or podonomine affinities in rich oil shale from the Green River Formation ( Eocene) of Wyoming ( x296 ). than twice the diameter ( Fig. 7). Lengths of fecal pellets of third instar larvae are intermediate between those of the second and fourth instars. We also measured about 100 fecal pellets taken at random from the sediment surface in Mud Lake. These had an average diameter of 0.142 mm and an average length of 0.364 mm. Their slightly smaller average diameter reflects the presence of pellets f.rom earlier instar larvae. The fact that fecal pellets not identifiable as those produced by chironomids are negligibly few leads us to conclude that the sediment was produced by chironomid fecal pellets to the viitual exclusion of all other forms. FIG. 9. Photomicrograph of a fossil, but unmincralized, chironomid pupa having tanypodine or podonornine affinities in rich oil shale from the Green River Formation (Eocene) of Colorado. At a are two respiratory horns attached to fragment of the head of another tanypodine pupa ( x16). LACUSTRINE CONCLUSIONS COPROPEL IN MUD LAKE 905 pelletal organic ooze in Gosiutc and Uinta lakes of some 50 million years ago to that the living chironomids play today in producing the fecal pcllct ooze of Mud Lake sedimcnts. These studies suggest that blue-green algae are prerequisite to the formation of copropel similar to that accumulating in Mud Lake. Were there a significant proREFERENCES duction of small planktonic green algae, 1964.) The Rift Valley R. S. A. they, too, would surely be harvested by the BEAUCHAMP, Iritern. Ver. Thcoret. Angew. lakes of Africa. chironomids, but after passing through the Limnol. Vcrhandl., 15: 91-99. intestines of the larvae their remains pre- BRADLEY, W. H. 1966: Tropical lakes, copropel, sumably would be dispersed and recircuand oil shalt. Bull. Geol. Sot. AI?., 77: lated into the water column and would not 1333-1338. AND M. E. BEARD. 1969. Mud Lake, accumulate in the sediment as do the blue- Flbrida; its algae and alkaline brown water. greens. The apparent paucity of the benLimnol, oceanog., 14: 889-897. thos and particularly the small populations FISII, G. R. 1955. The food of TiZupiu in East of Chironomidae suggest that predation is Africa. Uganda J., 19: 85. extreme, whereas low diversity of the Chi- HICKLING, C. F. 196,l. Tropical inland fisheries. Longmans, London. 287 p. ronomidae at this latitude may be attributed to the fact that few organisms arc able to JONASSON, I?. M. 1961. Population dynamics in Chironomus anthracin,us Zett. in the profundal tolerate conditions existing in such shallow zone of Lake Esrom. Intern. Ver. Theoret. lakes. Angcw. Limnol. Verhandl., 14: 196-203. LATIMQ W. L., AND R. G. ANDIWON. 1965. The extent to which the richly organic Some algae isolated from casts of earthworms. sediment of Mud Lake can be regarded as Am. J. Botany, 52: 653. a good model for the richly organic lacusPIIATT, R. 1942. Studies on ChZorellu vulgaris. trine sediments that must have served as V. Some properties of the growth inhibitor precursors of the oil shale beds of the Green formed by ChloreZZa cells. Am. J. Botany, 29 : 142-148. River Formation (Eocene) cannot yet be 1943. Studies on Chlorella vulgaris. VI. fully assessed. Nevertheless, several of our -. Retardation of photosynthesis by a growthresults strengthen the impression that the inhibiting substance from ChZore2Za vulgaris. analogy between Mud Lake sediment and Am. J. Botany, 30: 32-33. at least some ancient oil shale precursors -. 1944. Studies on Chlorella vulgak. IX. Influence on growth of Chlorella of continuous is good. One of these is the fact that a removal of chlorellin from the culture solution. copropelic structure much like that in Mud Am. J. Botany, 31: 418-42,l. Lake sediment is discernible in some thin -, T. DANIELS, J’. EILER, J. GUNNISON, W. sections of rich oil shale, and we understand KU~VLER, J. ONETO, L. STRAIT, H. SPOFXIR, G. now why Mud Lake sediment has a wholly HARDIN, H. MILNER, J. SMITEI, AND H. STRAIN. 1944. Chlorellin, an antibacterial substance pelletal structure. Even more convincing is from Chlorella. Science, 99: 351-352. the fact that many rich oil shale beds in the J. ONE~TO, AND J. PRATT. 1945. Studies Green River Formation of Wyoming and -, on Chlorella vulgaris. X. Influence of the age Colorado contain numerous unmineralized of the culture in the accumulation of chlorellin. remains of midge larvae ( Fig. 8) and pupae Am. J. Botany, 32: 405-408,. ( Fig. 9). Although it is impossible on the PROCTOR, V. W. 1959. Dispersal of fresh-water algae by migratory water birds. Science, 130: basis of these fossils to identify the midges, 623-624. two things are obvious : 1) the remains RYTHER, J. H. 1954. Inhibitory effects of phytoappear to represent several taxa, and 2) plankton upon the feeding of Daphnia magna these forms, although not similar to known with reference to growth, reproduction, and survival. Ecology, 35 : 52%533. species on this continent or abroad, have SWAIN, F. M., AND N. PI~OKOPOVICFI. 1954. Stratichironomine, orthocladiine, and tanypodine graphic distribution of lipoid substances in affinities. These ancient chironomids eviCedar Creek Bog, Minnesota. Bull. Gcol. dently played a similar role in producing Sot. Am., 65: 1183-1198.