Download the role of larval chironomidae in the production of lacustrine

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.