Things reveal, in their forms, in their movements,
the processes that shaped them, as the rocks reveal
in their roundness and their crevices
the movement o water.
Starhawk
Dreaming
AN ABSTRACT OF THE THESIS OF
Rosanna L. Mattingly for the degree of Doctor of Philosophy in
Fisheries and Wildlife
presented on
July 2, 1985
Title: Troph c and Habitat Requirements of Two Deposit-Feedi
Stream Inver ebrates, Ptychóptera townesi (Diptera) and
paraleptophi bia spp. (Ehemerotera)
Abstract approved;
Redacted for privacy
Chailes E. Warren
Ptychoptera townesi (false crane fly, Diptera) occur in
high densities in an experimental stream section that has not
been allowed to exceed bankfull flow for more than two decades,
but are quite rare in areas both upstream and downstream from
this section.
By contrast, ParaleptophJ.ebia spp. (mayfly,
Epherneroptera) are relatively abundant throughout the channel.
Paraleptophiebia spp. are able to feed and grow on a variety of
resource types, whereas Ptychoptera townesi are restricted to
feeding on fine particulate organic matter (FPOM) less than 250
urn in diameter, particularly 0.45-53 urn.
Morphological and
behavioral differences between these genera are indicative of
differences in feeding capability.
These genera also differ in response to refractory food
resources.
The alimentary tract of the dipteran is considerably
more differentiated than the simple straight tube gut tract
typical of the mayflies.
In addition, Ptychoptera townesi
consume relatively small amounts (per unit animal dry mass) of
particulates (0.45 - 53 urn) compared with the mayflies
ingestion of leaf material.
Ptychoptera townesi have longer gut
content passage times (> 19 h) and higher efficiencies of
conversion of ingested substrate to body substance, under
conditions studied, than do Paraleptophlebia spp.
these respective food resources.
(2-3 h) on
Gut contents of Ptychoptera
townesi become colonized by microbes typically found in the
hindgut, and are compacted into pellets considerably larger in
size than particles ingested.
These animals lose mass when
allowed to feed on this material.
Ptychoptera townesi ingest
and egest relatively sterile detrital material at a rate reduced
from that on natural detritus.
The pattern exhibited by Ptychoptera townesi involves slow
handling of relatively small volumes of food, which probably
pass once through an elaborate alimentary tract.
That exhibited
by Paraleptophiebia spp. involves rapid processing and partial
recycling of large amounts of material through a relatively
simple alimentary tract.
Considered in a broader context, the
results of this investigation have implications for the
perceived role of deposit-feeding organisms in the organization
and development of stream communities.
Deposit-feeders are
capable of far more than, as generally claimed, selecting
particles on the basis of size, independent of food quality, and
digesting primarily the associated microbes for their nutrition.
Trophic and Habitat Requirements of Two Deposit-Feeding
Stream Invertebrates, Ptychoptera townesi (Diptera)
and Paraleptophiebia spp. (Ephemeroptera)
by
Rosanna L. Mattingly
A THESIS
submitted to
Oregol) State University
in partial fulfillment of
the requirements for the
degree of
Doctor of Philosophy
Completed July 2, 1985
Commencement June 1986
APPROVED:
Redacted for privacy
Proesso?f Fisèries and Wildlife in charge of major
Redacted for privacy
Head of deçatmènt of iédWiTdI1fè
Redacted for privacy
n ot Gractute
Date thesis is presented
July 2, 1985
Typed by Rosanna L. Mattingly for
Rosanna L. Mattingly
to my parents
VINCENT and DOLA MATTINGLY
AC KNOWLEDGMELTS
I want to express my heartfelt gratitude to Charles
Warren, my major professor, for his kindness,
encouragement, and support throughout the various phases
of my education and development at Oregon State.
The
integrity and whole-mindedness with which he persues his
own goals have influenced my beliefs and feelings about
living as much as they have about doing science.
My
experience has been enriched also through interactions
with other members of my graduate committee: Alan Berg,
Kermit Cromack, Jr., Harry Phinney, and Richard Tubb.
Each of them has contributed to my understanding of
science as a human endeavor.
Numerous colleagues and friends participated in
countless ways in my growth during the years of this
study.
Although I do not acknowledge each by name, I am
sincerely grateful to all of them.
George Lauff and Mike
Kiug provided computer and laboratory facilities at
Kellogg Biological Station7 Bill English and Kelly Moore
assisted with field collections; Karan Fairchild ashed
numerous substrates; Peter westigard and Ralph Berry
kindly allowed me use of word processors; and John Gill
provided statistical consultation.
I thank, with much love, Vic Bogart, JoAnn
Burkholder, Larry Gut, Gael Kurath, and Carol Spears.
They have given far more, intellectually, emotionally, and
spiritually, than I ever could have asked.
And a very
special thank you, with love and respect, to my family --
Mom and Dad, my sisters sandy and Tern, and my brothers
Bruce and Vincent.
At times they knew me better than I
knew my self, and always had a way of "being there" when I
needed.
(Bracken, too!)
This research was funded primarily through the
Department of Fisheries and Wildlife, Oregon State
University.
TABLE OF CONTENTS
INTRODUCTION
1
MATERIALS AND METHODS
Organisms
Primary Collection Sites
General Experimental Design
Macroinvertebrate and Substrate Analyses
Procedure for tracking animals and
determination of mass
Growth rate determination
Consumption and efficiency indices
Gut content passage time
Egestion
Substrate particle size distribution
Organic content
Microscope studies
Statistical Analyses
9
9
9
RESULTS AND INTERPRETATION
Habitat Requirements
Berry Creek substrate
Relative mobility of animals
Relative animal distribution
Trophic Requirements
Resource type and particle size
Effects of environmental alteration
Mouthparts
Alimentary tracts
Food handling: consumption
Food handling: gut content passage time
Food handling: assimilation
Food handling: egestion
Recycling of fecal material
Life History
Summary of Trophic and Habitat Requirements
and Life Histories
11
13
13
14
15
16
17
18
18
18
19
21
21
21
22
23
28
28
34
40
45
49
52
55
57
61
68
71
DISCUSSION
74
LITERATURE CITED
85
LIST OF FIGURES
igure
1.
2.
Interrelationships among morphological,
behavioral, and physiological constraints
on survival and growth of deposit-feeding
organisms.
7
scanning electron nicrographs of the head
capsules of Ptychoptera townesi (a at 200x)
and Paraleptophlebia sp.at lOOx), and
their respective mandibles (c at 500x and e
at l000x, d at 200x). A inaxilla of the
mayfly is shown in f (200x).
3.
4.
5.
41
Photographs (a) of red alder leaf disks fed
on for 1 - 2 h by Paraleptophiebia spp. and
(b) of Ptychoptera towrlesi and Paraleptophlebia spp. wi?Efeces (the false crane
fly egests the larger particles). Scanning
electron micrographs of the fecal pellets
of Ptychoptera townesi. (c at 200x) and
Paraleptophiebia spp. (d at 500x), and
respective secEions from each (e and f at
2000x).
43
Alimentary tracts of (left) Ptychoptera
townesi and (right) Paraleptophiebia sp.
f = foregut; gc = gastric ceca; h = hindgut;
i=ileum; ls=lime sac; mt=Malpighian tubules;
o=esophagus; p=proventricuius; r=rectum;
s = salivary gland; v= ventriculus or
midgut (differentiated according to
Wigglesworth 1972).
46
Egestion rates (mg/animal/h) of Ptychoptera
townesi.
(a) Food available continuously,
(b) animals removed from substrate prior to
u:;urement, (c) Food available initially
but animals removed frou ubs;trate (arrow)
after a period of feeding.
59
LIST OF TABLES
Table
1.
2.
3.
4.
5.
6.
7.
8.
Page
Details of experimental design of
individual trophic investigations, and
estimated mean initial dry mass (± standard
deviation) of experimental animals.
12
Size distribution and organic content of
particles less than 1 tan in diameter (mean
percentage ± standard deviation) from Berry
Creek (Beriori County, Oregon) riffles and
pools both upstream from and within the
flow-controlled portion of the channel.
22
Mean percentage organic content (± standard
deviation) of substrates collected from
habitat types within the flow-controlled
section of Berry Creek (Benton County,
Oregon).
23
General habitats
Ptychoptera (ten
and of the genus
species in North
of larvae of the genus
species in North America)
Paraleptophlebia (33
America).
26
Comparative survival and growth (mean ±
standard error) of Ptychoptera townesi and
Paraleptophiebia spp. on coarse and fine
?articulate organic matter (Experiment 1).
29
Survival and growth (mean) of Ptychoptera
townesi (± standard deviation) and Paraleptophlebia spp. (± standard error) on FPOM
size fractions of ground, leached alder
particlAs (Experiment 2).
32
Relative growth rates (mean ± standard
error) and survival of Paraleptophlebia
spp. on particle size fractions of sediment
from Oak Creek (Experiment 3).
33
Relative growth rates and mean final dry
masses (± standard error) of early instar
Paraleptophiebia spp. on particle size
fractons of Berry Creek sediment
(Experiment 4).
35
Table (cont.)
9.
10.
11.
12.
13.
14.
15.
16.
Page
Growth (mean ± standard error) and survival
of Ptychoptera townesi on sediments (53 250 urn) collected from the relatively
undisturbed Trap Bay Creek drainage,
Chichagof Island, Alaska (Experiment 5).
36
Survival and growth (mean ± standard error)
of Ptychoptera townesi on sediments
collected from variously disturbed sites on
Mount St. Helens (Experiment 6).
37
Survival and growth (mean ± standard error)
of Paraleptophlebia spp. on sediments from
progressively affected sites on Mount St.
Helens (Experiment 7).
39
Consumption rate (CR), consumption index
(Cl), and efficiency of conversion of
ingested food to body substance (ECI) (mean
± standard deviation) for Ptychoptera
townesi on UPOM and Paraleptophiebia spp.
on alder leaves.
50
Daily (mg/d) and relative (mg/mg/d) rates
of egestion (mean ± standard error) by
Ptycptera t8wnesi an Paraleptophiebia spp.
at 4 C and 10 C.
58
Survival and growth (mean ± standard error)
of Ptychoptera townesi and Paraleptophiebia
spp. on UPOM and alder leaves from Berry
Creek, and on feces collected from Ptychoptera
townesi feeding on UPOM (Experiment 8).
64
Survival and growth (mean ± standard error)
of Ptychoptera townesi and Paraleptophiebia
spp. on alder leaves, alder leaves with
shredders (Lepidostoma sp. and Zapada sp.),
and feces from shredders (Holorusia sp.)
which were fed alder leaves (Experiment 9).
66
Survival and growth (mean ± standard error)
of Ptychoptera townesi and Paraleptophiebia
spp. on alder leaves and on feces from
shredders (Holorusia sp.) fed alder leaves
(Experiment 10).
67
Table (cont.)
Page
Information concerning voltinism and
emergence, oviposition, and fecundity of
the genera Ptychoptera and Paraleptophiebia.
69
18.
Potential bases for detritivore nutrition.
75
19.
Commonly used measures of food quality.
76
20.
Options of detritivores feeding on a
nutritionally poor resource.
78
17.
TROPHIC AND HABITAT REQUIREMENTS OF TWO DEPOSIT-FEEDING
STREAM INVERTEBRATES, PTYCHOPTERA TOWNESI (DIPTERA) AND
PARALEPTOPHLEBIA SPP. (EPHEMEROPTERA)
INTRODUCTION
Deposit-feeding organisms in freshwater systems feed
on fine particulate detritus, and are generally
conceptualized as part of what Swift et al. (1979) term
"the detritus community," taxa involved in the production
and consumption of detritus.
Processes involved in the
development and maintenance of this system have been
detailed by Dickinson and Pugh (1974), Anderson and
Macfadyen (1976), and Swift et al. (1979).
Recognition of subgroups, such as deposit-feeders,
associated with detritus is often based on behavioral and
morphological adaptations to feed on either coarse
particulate organic matter (CPOM; material greater than 1
mm in particle diameter) or fine particulate organic
matter (FPOM; material that ranges from 0.45 urn to 1 mm in
particle diameter)(Cummins 1974).
According to the
category of particle size on which they feed, then, large
detritivores have been trophically classified as
coarse-particle feeders (shredders) or as fine-particle
feeders (collectors: filter-feeders and deposit-feeders)
(Cummins and Kiug 1979).
Fine particulate organic matter provides an abundant
2
(Sedell et a].. 1978; Gurtz et al. 1980; Cummins et al.
1981) and relatively stable (Levinton 1972) nutritional
and habitat resource for stream organisms.
Even SO?
neither qualitative change during processing (e.g.,
Mattingly ms) nor the utilization of detrital material
(Hynes 1970; Cummins and Kiug 1979) in stream systems is
well understood.
The 0.45-urn lower particle size range
limit of FPOM is the Millipore filter size conventionally
chosen to separate fine particulate (FPOM) from dissolved
organic matter (DOM; material less than 0.45 urn in
particle diameter).
The 1-mm upper limit is an
arbitrarily determined cut-off between fungi-dominated
systems (cPoM) and systems colonized predominantly by
bacteria (FPOM; M.J. Kiug, personal communication; Cummins
and Kiug 1979).
In this investigation, invertebrates that feed on
FPOM in stream sediment are referred to as the
"deposit-feeder guild" in that they use the same
investigator-defined resource (MacMahon et a].. 1981).
The
particular use of, and effects upon, the FPOM resource by
specific taxa are not major criteria for this grouping
(see, however, Jaksi6 1981).
Habitat and life cycle
considerations, which are interrelated with trophic
adaptations, further differentiate this guild (e.g.,
Wevers 1983).
Organisms feeding on the FPOM resource generally have
.3
been assumed to select fine particulate organic matter on
the basis of particle size, independent of food quality -i.e., these animals are supposed to feed on anything as
long as it isof an appropriate, ingestible particle size
(Cununins and Spengler 1978; Cummins and Klug 1979).
The
reasoning behind this view involves the following four
arguments.
(1) Studies of filter-feeders such as Simuliidae and
Hydropsychidae have indicated that they filter particles
of little or no nutritional value (e.g., aluminum and
charcoal) from the water column until the animals die of
metabolic exhaustion (e.g., review by Wallace and Merritt
1980).
Ingestion of nonnutritious particles such as
charcoal, sand, or latex microspheres (as demonstrated by
Ladle et al. [1972], Mulla and Lacey [1976], and Wotton
[1976] for blackflies) cannot be taken as evidence against
selection (Becker 1958; Cummins 1973).
Nevertheless, it
has been used in this way and has been assumed to hold for
deposit-feeders as well.
(2) The time required for detritus to pass through
the alimentary tract is relatively short for many animals
that feed on the FPOM resource -- e.g., 20-30 mm
for
blackflies (Ladle et al. 1972), and less than 1 h for some
mayflies (Zimmerman and Wissing 1978; McCullough et al.
1979) and oligochaetes (Harper et al. 1981).
Because
assimilation efficiencies of animals feeding on detritus
4
have been measured to be relatively low
1%; Mattson
(
1980), these animals have been presumed to pass a low
quality substrate through the gut rapidly, and assimilate
only material (e.g., microbes) that is easily digested
(Bjarnov 1972; Cummins and Kiug 1979).
Time required for
discrimination among particle types would reduce time
otherwise available for ingestion of substrates.
(3) Many studies that purport to show selective
ingestion by deposit-feeding organisms are based on
comparative measurements of a food quality parameter of
the sediment and of the animals' feces.
If, for example,
the feces are of a higher nitrogen content than the
sediment, the animal may be said to have selected higher
quality particles from those available for ingestion
(Brinkhurst et al. 1972).
However, factors other than the
original composition of material ingested may affect the
nitrogen content of the feces.
(4) In a study of relative growth rates of the
deposit-feeding chironomid Stictochiroriomus annulicrus, in
which stream detritus was diluted with various proportions
of sand to simulate natural differences in relative food
quality (Mattingly et al. 1981), the inidges were unable to
maintain similar rates of relative growth.
This suggests
that the animals on treatments with the most sand were
unable to sort and select particles on the basis of food
quality.
However, an alternative explanation could
5
involve the animals' ability to alter the rate of
ingestion according to the relative quality of food
substrates.
It is possible that either they were not able
to increase the rate of ingestion enough to compensate for
differences in relative quality of the substrates to
maintain growth or they decreased or ceased ingestion of
relatively poor substrates.
Even though the claim that deposit-feeding organisms
ingest particles on the basis of size independent of food
quality is poorly substantiated, it has led to a related
generalization concerning the role of these organisms in
stream system dynamics.
Because of the relatively low
nutritional value of the particle substrate and the
overall abundance of relatively high quality bacteria, the
assumption has been made that deposit-feeders depend on
particle-surface bacteria for their nutrition (Bjarnov
1972; Anderson and Cummins 1979; Cummins and Kiug 1979;
Saunders 1980).
The generalized "particle stripping
hypothesis" (Saunders 1980) proposes that ingested fine
detrital particles and microbes may be packaged in fecal
pellets to be defecated, recolonized, and processed by
inter- and intraspecific coprophagy.
Continued processing
generates particles that differ in size, age, and degree
of recalcitrance.
Multiple, repetitive processing of FPOM
is assumed to be the rule (Saunders 1980).
In stream
systems, the deposit-feeder guild in this view is
relegated to performing a task in the detrital "processing
line" (Pomeroy 1980).
As will be explored, maintenance of this view in the
absence of a complementary, broader perspective limits
attempts to understand adaptation of deposit-feeding
organisms to their food resource as well as their possible
roles in stream communities.
The major goal of this
investigation was to increase understanding of the trophic
dynamics of deposit-feeding organisms.
This was sought
primarily through examination of adaptations of
deposit-feeding organisms to their nutritional and habitat
resources, and the effects of substrate particle size and
quality on their survival and growth (Figure 1).
Habitat
requirements and other aspects of an organism's life
history are closely related to trophic aspects.
Thus,
habitat and life cycle considerations of deposit-feeders
also were examined.
The number and diversity of deposit-feeding organisms
prohibits extensive study of all taxa.
The detailed
investigations reported here focus on two genera of
deposit-feeders, Ptychoptera townesi Alexander
(Ptychopteridae; Diptera) and Paraleptophiebia spp.
(Leptophlebiidae; Ephemeroptera), that differ in habitat,
life history, and trophic requirements and patterns.
Figure 1.
Interrelationships among morphological,
behavioral, and physiological constraints on
survival and growth of deposit-feeding
organisms.
Food Resource
Feeding
Morphology
Behavior
Consumption
/
Gut Tract
/ Morphology
Microbiology
Biochemistry
Assimilation
Gut Content
Passage Time
I
II,
Feces
Figure 1.
Egestion
Growth
Survival
(Reproduction)
MATERIALS ANI) METHODS
Organisms
Larvae1 of Ptychoptera townesi Alexander (false
crane fly; Diptera) and of Paraleptophiebia gregalis
(Eaton) and Paraleptophiebia temporalis (McDunnough)
(mayflies; Ephemeroptera) were used in studies described
in this paper.
The mayflies were considerably more
sensitive to handling and temperature change than were the
false crane fly larvae.
All animals were kept cool and
aerated during transport from collection sites to nearby
laboratories.
Animals used in studies completed in more
distant laboratories were shipped (in plastic bags filled
with water and packaged in blue ice and styrofoam)
so that
they arrived within 24 h after the time of collection.
Primary Collection Sites
Ptychoptera townesi used in trophic studies were
collected from depositional areas, and Paraleptophiebia
spp., from both erosional and depositional areas of a
flow-controlled section of the North Fork of Berry Creek
and from Oak Creek and a small tributary to Oak Creek.
Two additional mayfly species,
Paraleptophlebia bicornuta
McDunnough and Paraleptophiebia debilis (Walker)
(identified respectively by mandibular tusks and barred
1Larva is used to refer to the immature feeding stage of
both hemimetabolous and holometabolous species.
10
legs [Needham et al. 1935]), were eliminated from
collections.
Oak Creek and the North Fork of Berry Creek are
low-gradient, second-order streams located in Benton
County in the Willamette Valley of Oregon.
These streams
lie in second-growth Douglas fir (Pseudotsuga menziesii)
forest and have a riparian vegetation primarily consisting
of red alder (Alnus rubra)
inacrophyllum).
and bigleaf maple (Acer
Cottonwood (populus trichocarpa), Oregon
ash (Fraxinus oregona), and Oregon oak (Quercus garryaria)
also are relatively abundant.
Ninebark (Physocarpus
capitatus) and California hazel (Coryi.us rostrata var.
californica) are common riparian shrubs.
Clay strata
provide an abundance of colloidal materials to both
streams.
Further description of the vegetation and the
geologic setting of Berry Creek is provided in Kraft
(1964) and Warren et al. (1964).
A diversion dam and bypass around a 1500-ft (457.2-rn)
section of the Berry Creek channel (Warren et al. 1964)
were constructed in the late 1950s.
The flow-controlled
section (i.e., that which is bypassed) carries discharges
up to bankfull flow and the bypass channel carries the
overflow.
Thus, the flow-controlled section has
accumulated large quantities of FPOM.
Observations during
periods when upstream waters were blocked from the
flow-controlled section suggest that channel flow in
11
low-flow periods is maintained in large part through
groundwater interception.
General Experimental Design
Animals collected for growth studies were wet weighed
and either measured for total length or sorted into size
classes, according to the animal species and size range
required for a particular experiment.
A subsample of
animals was oven dried and weighed at the beginning of
each experiment.
These measurements either provided
initial estimates of mean dry mass or were used in
developing a regression equation from which initial dry
masses were estimated according to measurements of total
length or mass of live animals.
Specific information for
individual experiments (e.g., temperature, duration,
laboratory apparatus used) and modifications of this basic
scheme are provided in Table 1.
The substrates employed in laboratory feeding and
growth experiments were either field collected or prepared
by grinding coarse particulate leaf material and allowing
particles to leach for 48 h in distilled water.
Substrates were wet-sieved through a Tyler screen series
to specified particle size fractions and incubated in
either 0.45 urn- or 53 urn-filtered stream water.
Except
where otherwise noted, stream substrates were collected
simultaneously and from the same sites as were the
12
Table 1.
Details of experimenta} design of individual
trophic investigations
and estimated mean
initial dry mass (± standard deviation) of
experimental animals.
,
Table Exper- Duration Temperiment
(days)
pparatus2 Repli- Estimated 4ean Initial
aure
ation
C)
Dry 1ass (mg) (n)
Ptychoptera
Paraleptotownesi
phiebia spp.
5
1
24
11
1
6
2
16
17
10
15
2
1
7
3
17
15
3.
8
4
42
11
1
17:1
9
5
54
15
1
15:4 0.08±0.02(53)
10
6
21
12
1
15:2 0.42*0.11(59)
10-12:3 3.67±0.93(53) 0.26±0.09(51)
0.40*0.11(48)
0.74*0.20(46)
1:12 5.37±2.08(32)
8;4
0.49±0.22(129)
8;4
0.49±0.22(129)
0.15*0.05(35)
0.58±0.14(59)
11
23
5
1
12
14
10
2
1;8-26 0.75*0.19(37) 0.39±0.18(40)
13
1
4
10
2
2
1;5-17 4.49±0.23(17) 0.54*0.27(4)
1:22-264.22±0.27(22) 0.65*0.06(26)
7
7;2
0.69±0.28(31)
14
8
26
12
1
10-15;2-3 4.37±1.44(36) 0.83±0.34(50)
15
9
34
10
3
3-5;4 5.34±1.45(76) 0.75±0.35(47)
16
10
24
10
1
3:4 5.85±1.33(66) 0.80±0.26(55)
1Light regimes simulating the field environment at the time the
animals were collected, and temperature control via incubator or cold
room were maintained during all laboratory experiments.
2i
aerated 500-mi. Ehrlenmeyer flasks; 2
f low-through chambers.
individually aerated vials; 3
3Number of animals per replicate; number of replicates per treatment.
4Mean initial dry mass estimates * standard error.
13
animals.
In feeding studies, animals are usually acclimated to
experimental conditions.
A comparison of percentage (by
dry mass) organic content of freshly collected animals
(Ptychoptera townesi: 75.7 ± 2.0%; Paraleptophiebia spp.:
97.8 ± 0.7%) versuè animals maintained under laboratory
conditions for a one-week period (Ptychoptera townesi:
76.7 ± 0.9%; Paraleptophiebia spp.: 96.4 ± 2.8%) indicated
that the period of holding did not noticeably affect
animal organic content.
In addition, animals monitored
for a two-week period under similar conditions, both in
the presence of and without food, showed no change in
either percentage (by dry mass) organic content or average
dry mass (unpublished data).
Experiments were generally
begun within 24 h of animal collection.
Macroinvertebrate and Substrate Analyses
Procedure for tracking animals and determination of mass
Large numbers of macroinvertebrates required handling
for drying, determination of mass, and/or ashing for
organic content.
Animals, individually or in small
groups, were transported in BEEM2 capsules permanently
engraved with a number by a diamond scribe.
Capsules were
maintained in sets of about 25 per container (e.g., Petri
2Better Equipment for Electron Microscopy, Inc., P.O.
Box 132, Jerome Avenue Station, Bronx, New York 10468
14
dish) in order to facilitate sorting and identification.
In addition, sets of unmarked capsules in labelled Petri
dishes were used for analyses in which groups of animals
rather than specific individuals were tracked.
Animals were dried on paper towels and placed in
capsules in an oven (50°C) for a period of time
sufficient to kill them (approximately 20 mm
- 1 h).
A
small puncture in the capsule lid prevented moisture from
condensing on the inside of the capsule.
After this
initial period, capsule lids were opened and the animals
were allowed to dry for a period of 24 h or longer,
according to the species and size.
Capsules were removed
from the oven, lids were closed, and then the capsules
were placed in a desiccator until they cooled to room
temperature.
Individual animals and animal fragments
(e.g., cerci or legs which often break off during
transport or the drying process) were, thereby, accounted
for in relatively limited space.
Masses of animals and
small substrate samples were determined on a Mettler M3
electrobalance.
A Cahn Model 9450 balance was used to
estimate masses of large substrate samples.
Growth rate determinations
Kirby-Smith (1976) suggests that the relative quality
of potential food materials can be assessed by measuring
the growth rates of animals fed these materials.
Growth
parameters and trophic indices (reported as mean ±
15
standard error) were calculated according to equations
given by Waldbauer (1968) and Cummins (1975):
Relative growth rate (RGR) = G/(TA), where
G = fresh or dry mass gain of animal during
feeding period
T = duration of feeding period (days)
= mean fresh or dry mass of animal during
feeding period
Relative growth rate x 100 = % change in body mass
per day.
Over short time intervals, RGR has been found to
approximate instantaneous growth rate (Cummins et al.
1973).
This was so in studies reported here.
Consumption and efficiency indices
For determinations of consumption rate (CR),
consumption index (CI), and efficiency of conversion of
ingested food to body substance (Ed), Ptychoptera townesi
were fed presieved Berry Creek UPOM (ultrafine particulate
organic matter; 0.45 - 53 urn in particle diameter) and
Paraleptophlebia spp. were given preleached alder leaf
disks.
The masses of these substrates were determined
after drying (50°C).
These substrates were placed in
aerated vials of filtered stream water prior to the
introduction of animals, which were allowed to feed for 14
days
(10°c).
Because fecal pellets produced by
Ptychoptera townesi were larger and those of
Paraleptophlebia spp. were smaller than the substrates
they ingested, materials were sieved at the conclusion of
16
the experiment to separate ingested from uningested
substrate.
Subsequently, substrates were redried and
their masses were determined.
Values for indices under
these laboratory conditions were calculated according to
the equations:
Consumption index (CI) = F/(TA), where
F
fresh or dry mass of food eaten
(other variables as above)
Consumption rate (CR) = mg (dry mass) food
ingested/day
Efficiency (percentage) of conversion of ingested
food to body substance (Ed) = RGR/CI or (larval dry mass
gained/dry mass food ingested) x 100
Vials containing only substrates were used to
estimate changes in mass owing to leaching, microbial
colonization, and experimental factors.
Preleached leaf
material was corrected for additional leaching loss on
wetting by a factor of 1.31% (± 1.13%; n=12).
Similarly,
sediments were corrected for experimental error owing to
incomplete recovery from the vials by 1.92% (± 0.41%; n9)
and for an additional sieving error of 0.43% (± 0.41%;
n=9).
Gut content passage time
Gut content passage times were measured with the aid
of a dye that binds to cellulose and is responsive to
ultraviolet radiation (M.J. Kiug, personal communication).
17
Animals were provided either dyed artificial substrates or
stream sediment mixed with dyed powdered cellulose.
Passage of the dye was then periodically evaluated by
epifluorescence microscopy.
In order to minimize
handling, gut content passage times were estimated for
Paraleptophiebia spp. (the more fragile of the species)
from the amount of material ingested during periods of
time less than that required to completely fill the gut.
An ultraviolet light source attached to a Wild M5
dissecting scope was used to observe gut contents of the
relatively larger Ptychoptera townesi.
Individuals of
this species were examined at 1-2 h intervals throughout
the period of time required for contents to pass through
the gut.
The effect of handling on the rate of food
ingestion and/or gut content passage time of these genera
is not known.
Egestion
Egestion rates were measured by allowing animals to
feed on unsieved Berry Creek sediment and then rinsing and
placing animals in individually aerated vials for a 24-h
period.
Animals were removed, and the contents of the
vials were filtered onto 0.45-urn Millipore filters.
Both
substrates and animals were dried at 50°C and their
masses determined on a Cahn electrobalance.
Egestion
rates were estimated according to the following equations:
Egestion rate (ER) = rng (dry mass) egested/day
18
Relative egestion rate (RER) = E/(TA), where
E = dry mass material egested
(other variables as above)
Substrate particle size distribution
Relative particle size distribution of Berry Creek
sediment was determined by wet-sieving sediment samples,
drying the material at 500C, and determining the mass
of the various size fractions.
These were subsequently
compared with the total dry mass of the initial sample.
Organic content
Organic contents of sediments, gut contents, feces,
and invertebrates were determined by drying samples at
50°C and ashing them at 5500C (Mattingly et al.
1981).
Subsamples treated with H202 to obtain a
measure of the clay-bound water fraction showed that this
fraction was quite variable.
Thus, corrections for this
were not practical.
Microscope studies
Substrates collected for examination by light (Madsen
1972) and epifluorescence microscopy (Madsen 1972;
Molongoski and Kiug 1976; Geesey et al. 1978) were kept
cool during transport to the laboratory, where they were
examined immediately.
Substrates examined by scanning
electron microscopy (Paerl and Goldman 1972; Suberkropp
and Kiug 1974; Geesey et al. 1978; Perkins and Kaplan
19
1978) were fixed in 3% glutaraldehyde solution with
Sørenson phosphate buffer.
Invertebrate mouthparts were
dissected from animals preserved in 70% ethyl alcohol,
either air dried or dehydrated in 100% ethyl alcohol, and
run through a dilution series.
The dilution series for
all samples consisted of 70:30; 50:50; 30:70 ethyl alcohol
to trichlorotrifloroethane (TF), to 100% TF, the
intermediate fluid.
Samples were critical point dried in
the transition fluid, freon-13 (monochiorotrifloroethane)
(Paerl and Shimp 1973; Lautenschlager et al. 1978),
mounted on stubs, vacuum-coated with a 60:40
gold-palladium alloy, and examined with a model AMR 1000
scanning electron microscope.
Observations were recorded
on Polaroid/Land film P/N Type 55.
Statistical Analyses
Data sets from growth studies were examined for
outliers (a = 0.01; test statistic = eL/
l-iiiI),
normality (a = 0.10; Shapiro-Wilk test using residuals),
and homogeneous variance (a = 0.2; Bartletts test) prior
to conservative analysis by a psteriori contrasts,
Tukeys test (J.L. Gill,personal communication; Gill
1978).
The modified test statistic used for experiments
with unbalanced replication was:
(
Vi )/4mse/r.
Analyses of variance and Bartlett's test were
4J
computed with Health Sciences Computing Facility,
University of California (Los Angeles), on VAX-ll/780,
running VAX/VMS version 3.1.
Data sets with normal
distribution but heterogeneous variance were analyzed by a
special Tukey-like procedure (Gill 1978).
21
RESULTS AND INTERPRETATION
Habitat Requirements
Berry Creek substrate
The relative size distribution of particles less than
1 mm in diameter and the percentage organic content of
each of the particle size fractions of sediment collected
from Berry Creek riffles and pools both upstream from and
within the flow-controlled portion of the channel are
presented in Table 2.
Material in the flow-controlled
section contains a relatively greater number of particles
less than 250 urn in diameter and relatively fewer
particles greater than 250 urn than does sediment in the
stream channel upstream from the bypass.
Particles less
than 250 um in diameter apparently have accumulated at a
greater rate in the flow-controlled section since the late
1950.
The flow-controlled section contains
quantitatively more FPOM than does the stream channel
either upstream or downstream from the bypass.
Such
material is 0.5 in deep in some depositional areas within
the flow-controlled section.
In addition, material in
depositional areas of the flow-controlled section of Berry
Creek contains relatively more organic matter than does
that in erosional areas (Table 3).
No seasonal change in
3However, water has gone over the dam several times during
intervening years (J. Lichatowich, personal communication).
22
Table 2.
Size distribution and organic content of
particles less than 1 nun in diameter (mean
percentage ± standard deviation) from Berry
Creek (Benton County, Oregon) riffles and pools
both upstream from an 3. within the flowcontrolled portion of the channel.
Substrate
location
ri
Particle size fraction
< 53 urn
53-125 urn
125-250
urn
250-500
urn
500
urn-i tam
Percentage of FPQM (less than 1 mm) portion:
Upstream from bypass:
Riffle 10
Pool
15.05(±3.04) 7.66(±l.55) 8.80(l.l4) 20.79(1.45) 47.71(i4.81)
8 13.20(*l.81) 8.76(*0.96) l0.22(i0.68) 28.11(2.29) 39.72(2.86)
Within flow-controlled gection:
Riffle
Pool
10 22.63(*3.54) 24.91(±1.68) 15.31(±l.17) 15.l0(±l.45) 22.07(±3.60)
8 37.67(*2.15) 28.59(±0.85) 19.97(l.47) 12.09(*1.87) l.68(0.23)
Percentage organic content:
Upstream from bypass:
Riffle
Pool
10 ].3.60(±1.45) l0.73(*2.06) 8.26(±0.95) 8.12(±0.79) 8.96(±0.70)
8 18.li(±0.65) 18.l9(3.96) 9.53(el.87) 8.93(±l.58) l0.21(±l.33)
Within flow-controlled section:
Riffle
Pool
10 15.40(*2.18) 19.59(±4.90) 15.83(±l.71) 21.79(*7.46) 15.26(2.56)
8 22.92(2.01) 33.86(*0.76) 43.32(*l.02) 49.84(±l.13) 64.15(±2.26)
23
Table 3.
Mean percentage organic content (± standard
deviation) of substrates collected from habitat
types within the flow-controlled section of
Berry Creek (Benton County, Oregon).
Type of Habitat
Substrateorganic
content
(%)
Erosional
channel
side channel
embedded stones
undercut bank
Depositional
under leaves
log jam
leaf pack
channel
moss
9.4
12.7
10.4
7.3
±
±
±
±
3.3
2.2
1.4
3.9
26.0
29.1
47.6
31.9
73.9
±
±
±
±
±
17.2
13.1
12.0
10.6
7.1
24
organic content of Berry Creek sediment was found.
Relative mobility of animals
Paraleptophiebia spp. are more mobile organisms than
are Ptychoptera townesi.
Paraleptophiebia spp. are
negatively phototrophic (Chapman and Demory 1963; Edmunds
et al. 1976), and orient facing into the current (personal
observation; Gilpin and Brusven 1970).
This orientation
is pronounced: the mayflies were observed to swim
vertically up the sides of circular chambers and to enter
tubing emitting water droplets into the chambers.
Ptychoptera townesi, on the other hand, simply burrow into
suitable substrates.
These diurnal organisms (Rogers
1942) have setae on annular thickenings that allow them to
advance by alternate expansion and contraction of segments
(Miall 1895).
They are very active in relatively inert
substrates such as sand or beads of cation exchange resin,
but burrow into and become inactive in fine silty
sediment, from which only their respiratory siphons
protrude into the water column.
Both genera are of a form (elongate and narrow)
suited for burrowing (Mynes 1970; Wagner 1978).
Ptychoptera townesi spend less time in the current than do
the mayf lies.
When disturbed, Ptychoptera townesi propel
themselves into the water column with a series of rapid
winds along the length of the body and come to rest in a
new location.
Levinton (1972) noted that obligate
25
deposit-feeders appear to be adapted to remaining within a
circumscribed area rather than being carried by the
current.
Paraleptophiebia spp. swim up into the water
column in a wavelike motion when disturbed.
are less active in the sediment.
The mayf lies
They often lie flush
with the substrate and become buried with fine particles.
Relative animal distribution
Ptychoptera townesi are rare in occurrence in Berry
Creek both upstream and downstream from the
flow-controlled channel, yet these animals are very
abundant within depositional areas of the channel section
where particles less than 250 um in diameter have
accumulated (unpublished data).
This suggests that
habitats in this section are particularly well suited for
false crane fly larvae, and is in agreement with the
findings of other investigators (Table 4).
By contrast,
estimates of Paraleptophiebia spp. density in the
experimental and upstream sections of the stream are
similar (unpublished data).
Changes in particle size
distribution, quality, or other factors related to lack of
flooding appear not to affect the distribution of
Paraleptophiebia spp. as much as that of Ptychoptera
townesi.
This is consistent with other studies that
indicate leptophlebiid mayflies of the genus
Paraleptophiebia generally inhabit areas of relatively
swift current where reduced accumulations of fine
26
Table 4.
General habitats of larvae of the genus
ptychoptera (ten species in North America) and
of the genus Paraleptophiebia (33 species in
L'Torth America).
Ptychoptera spp.
Habitat
Reference
Para1eptopilebia spp.
Habitat
Reference
Decaying vegetation
in shallow water
1,3,4,5,7,10,
11,15,16,18
Swift water, slowly
to moderately flowing riffles
Organic sediment
l,3,5,7,19,20,P
Leaf debris
l0,17,P
Springs. and slowly
flowing streams
l0,P
Tops and sides of
rocks
13, P
Bogs (PR 4-5.6)
4
Beneath rocks
9, l7,P
Tributary mouths
(areas of high Fe
concentration)
12,21, P
Bittacomorpha, a
23
related genus, has
widespread distribution
in North America
Holarctic distribution.
In Nearctic,
general throughout
North America
8,10,13,14
17,22,P
6
1. Mial]. 1895; 2. Topsent 1914-16; 3. Alexander 1920; 4. Rogers 1933;
5. Johannsen 1934; 6. Needham et a).,
1935; 7. Peterson 1960; 8.
Leonard and Leonard 1962; 9. Cffpn and Demory 1963; 10. Kraft 1964;
11. Kiots 1966; 12. Mackay 1969; 13. Gilpin and Brusven 1970; 14. Rynes
1970; 15. Wirth and Stone 1971; 16. Hodkinson 1973; 17. Edmunds et a]..
1976; 18. Pennak 1978; 19. Wagner 1978; 20. Tolkamp 1980; 21. Harris
et a).. 1981; 22. Pereira 1981; 23. Merritt and Cummins 1984; P. Present
study.
27
particles occur (Table 4).
however, note that
Lehm]cuhl and Anderson (1971),
Paraleptophlebia temporalis occur in
riffle areas in Oak Creek from August to November, but
move to slower water as they mature.
Relative densities of animals in riffle and pool
areas of Berry Creek suggest that larvae of Ptychoptera
townesi and Paraleptophiebia spp. differ in their
requirements and ability to colonize stream habitats.
This is supported by studies with artificial stream
channels (described by Wevers 1983).
Ptychoptera townesi
enter the channels, but do not become established in
either erosional or depositional substrates.
Deposits in
the artificial channels are shallower than those in the
Berry Creek experimental channel.
Paraleptophiebia
gregalis and Paraleptophiebia temporalis enter the
channels and colonize both riffle and pool areas (M.J.
Wevers, unpublished data).
Given these differences in habitat, the relative size
and quality of FPOM available to these animals in nature
may differ as well.
As noted (Tables 2 and 3), particle
size distribution and organic content of sediment in
riffle areas are not the same as those in pools.
Animals
presumably are usually associated in nature with food
resources to which they are well adapted.
Organic
substrates such as FPOM and leaves provide habitat as well
as
nutritional resources for deposit-feeders.
28
Trophic Requirements
Resource type and particle size
Larvae of Ptychoptera townesi and Paraleptophiebia
spp. were allowed to feed on FPOM and CPOM collected from
Berry Creek.
The FPOM consisted of two size categories,
one 0.45-53 urn in diameter (UP0M) and the other 53-250 urn
in diameter.
Invertebrate growth rates and percentages of
survival and substrate organic contents are presented in
Table 5 (Experiment 1).
The false crane fly larvae grew
on UPOM and lost a significant (a < 0.05) amount of mass
on conditioned alder leaves as compared with UPOM.
Growth
rates of Paraleptophiebia spp. on the leaf material were
significantly (a < 0.01) higher than were their growth
rates on either of the FPOM categories.
Measures were
made of growth on periphyton (20.2% organic content) at
the same time and under the same experimental conditions
as on FPOM and leaves.
Periphyton is abundant in stream
riffle areas where Paraleptophlebia spp. occur.
Ptychoptera townesi lost mass (-1.77 ± 0.81% body wt/d,
27% survival), whereas the mayflies were able to maintain
their mass (0.05 ± 0.95% body wt/d, 56% survival) on this
substrate.
False crane fly larvae apparently are more
restricted as to resource type than are the mayflies.
Ptychopterids generally have been reported to feed on
sediment and decaying vegetation (Alexander 1920; Rogers
29
Table 5.
Substrate
UPOM
Comparative survival and growth (mean ± standard
error) of Ptychoptera townesi and Paraleptophiebia spp. on coarse and fine particulate
organic matter (Experiment 1).
Substrate
Ptychoptera townesi
Paraleptophlebia spp.
organic
content Survival Relative growth Survival Relative growth
(%)
(%)
rate(% body wt/d)
(%)
rate (% body wt/d)
21.9
90
27.2
100
-0.44 ± 0.26
53
0.57 ± 0.30
85.4
87
-0.82 ± 0.19
79
3.31 ± 0.24
0.35
0.20
47
(0.45-53 urn)
FPOM
(53-250 urn)
Alder leaves
033 ± 0.23
30
1933; Kiots 1966; Pennak 1978; Wagner 1978; Tolkamp 1980).
Paraleptophiebia spp. also are considered to be primarily
detritivores (Kraft 1964; Gilpin and Brusven 1970; Edmunds
et al. 1976; Shapas and Hilsenhoff 1976; Pereira 1981).
Mayf lies of the related species Leptophlebia cupida are
fine particle detritivores and have been reported to
ingest particles averaging 38 urn in diameter (Clifford et
al. 1979).
Edmunds et al. (1976) report that most
Ephemeroptera genera, including many Leptophlebiidae, are
fine-sediment collectors or feed on fine detritus in
surface deposits, whereas they know of no genera in the
shredder category.
The Paraleptophlebia spp. I studied
are able to ingest coarse particulate material and do not
conform to this generalization.
Particle size categories include other physical and
chemical features, and natural stream sediments may
comprise ranges of particle size that differ in quality.
In order to separate potential particle quality effects in
feeding experiments from those related to particle size
(e.g., increasing organic content of sediment with
increasing particle size), particle substrates were
prepared from ground, leached, red alder leaves.
This
restricted substrates to the same type and, despite
differences in particle size and potential differential
microbial colonization, generally comparable and
relatively high nutritional value (Iversen 1974; Otto
31
1974; Petersen and Cummins 1974; Anderson and Grafius
1975).
Ptychoptera townesi feeding on these particles
(Experiment 2, Table 6) maintained approximate body mass
on substrates 53-125 urn in diameter, but significantly (a
< 0.01) lost body mass on particles in either of the
larger size ranges.
Morphological and feeding studies
reported in following sections indicate that these animals
are unable to ingest the larger particles.
Paraleptophlebia spp., when provided alder in
different ranges of particle size maintained approximate
body mass on particles 250-500 urn, but lost body mass on
other particle size ranges (Table 6), although differences
were not statistically significant (a < 0.05).
The
largest particles used in Experiment 2 lie at the upper
end (1
miii)
of the FPOM category, but are smaller than leaf
material used in other experiments (e.g., Experiment 1).
No significant differences were found between any of the
growth rates of mayflies fed particles of more defined
size ranges from Oak Creek, although mean growth rate was
lowest on the largest particles, 1-4 mm (Experiment 3,
Table 7).
Generally, Paraleptophiebia spp. growth on
particles of various size ranges, both with alder
particles and with natural substrates, did not exhibit any
general pattern of increase or decrease with particle size
(e.g., Experiments 1-3).
This was so even for early
32
Table 6.
Survival and growth (mean) of Ptychoptera
townesi (± standard deviation) and Paraleptophiebia spp. (± standard error) on FPOM size
fractions of ground, leached alder particles
(Experiment 2).
Ptychoptera townesi
Alder particle
size range (urn)
Surviva1
(%)
Paraleptophlebia spp.
Relative growth
Survival
rate (% body wt/d)
(%)
Relative growth
rate (% body wt/d)
53-125
100
-0.06 ± 0.77
---
ND
125-250
100
-1.80
0.86
100
-0.71 ± 0.79
250-500
67
-2.21 ± 0.91
100
0.18 ± 0.61
Ni)
75
-0.53 * 0.66
500-1 nun
---
*
Organic content, 89-92%. Substrate respiration values higher than those
measured for natural stream sediment within all stated particle size ranges.
33
Table 7.
Relative growth rates (mean ± standard error)
and survival of paraleptophiebia spp. on
particle size fractions of sediment from Oak
Creek (Experiment 3).
Substrate
particle size
range
Substrate
organic content
Animal
survival
(%)
(%)
Relative
growth rate
(% body wt/d)
53-125 urn
11.2
25
1.82 * 1.18
125-250 urn
13.7
75
1.59 ± 0.63
250-500 urn
9.3
25
1.48 * 0.57
500 urn-i mm
9.6
25
1.88 ± 1.73
84.6
75
0.81 ± 0.81
1-4 mm
34
instar Paraleptophlebia spp. (Experiment 4, Table 8),
which would be the most likely to be limited
morphologically to a small particle size range of the FPOM
resource.
Effects of environmental alteration
Differences were observed in growth rate and survival
of false crane flies provided sediments collected from a
number of streams in the relatively undisturbed Trap Bay
Creek drainage, Chichagof Island, Alaska (Table 9).
These
correspond generally with qualitative site descriptions
and observations (unpublished data).
Substrates on which
organisms exhibited high rates of growth contained
relatively more detrital material, whereas those on which
animals had reduced growth rates had relatively large
amounts of mineral material.
In order to compare the response of Ptychoptera
townesi with that of Paraleptophiebia spp. to substrate
alteration, individuals of both genera were presented
sediments collected from streams variously affected by the
eruption of Mount St. Helens.
False crane fly larvae grew
when provided sediments from the least disturbed sites,
and lost body mass or did not survive at all on sediments
from sites that were more affected by the blast (Table 10,
Experiment 6).
The relative growth rates of Ptychoptera
townesi fed the 53-125 urn particle size fractions from Elk
Creek, Middle Clearwater, and Upper Clea.rwater Creek were
35
Table 8. Relative growth rates and mean final dry masses
(± standard error) of early instar Paraleptophiebia spp. on particle size fractions of Berry
Creek sediment (Experiment 4).
Substrate
particle
size
range
Substrate
organic
content
Animal
survival
1ean final
dry wt (mg)
Relative growth
rate (% body wt/d)
(%)
(%)
< 53 urn
19.5
59
.133 * .010
-0.28
53-250 urn
16.7
82
.245 ± .022
1.14
250-500 urn
14.6
53
.413 ± .055
2.22
500 urn-i mm
20.1
59
.205 ± .020
0.74
36
Table 9.
Site
Growth (mean ± standard error) and survival of
Ptychoptera townesi on sediments (53 - 250 urn)
collected from the relatively undisturbed Trap
Bay Creek drainage, Chichagof Island, Alaska
(Experiment 5).
Substrate
organic content
Survival
(%)
Relative growth rate
(% body wt/day)
(%)
Muskeg Creek
24.1
78
2.80
0.28
5.4
53
2.20
0.20
Upper Control 18.2
Creek
63
2.05 ± 0.21
Lower Right
Fork
7.6
35
1.87 * 0.35
Lower Beach
Creek
13.9
30
1.41 ± 0.52
5.4
ii.
0.83 ± 0.69
Upper Left
Fork
Lower Trap
Bay Creek
37
Table 10.
Survival and growth (mean ± standard error)
of Ptychoptera townesi on sediments collected
from variously disturbed sites on Mount St.
Helens (Experiment 6).
Site
Substrate
particle size
range (urn)
Elk Creek
Substrate Survival
organic
(%)
content (%)
Relative growth rate
(% body wt/d)
53-125
l25 250
0.40
0.26
93
57
1.15
0.38
Upper Clearwater 53-125
125-250
0.23
0.25
3
0.74
Middle
Clearwater
125-250
1.03
1.61
83
10
53-125
125-250
0.18
0.17
0
53-125
125-250
0.16
0.18
(least affected
Muddy River
Ape Canyon
53-3.25
0.09
0.26
0
3
0.64 j 0.13
-0.68
-2.09
0
0
(most affected
*
Personal observation; K.W. Cummins, personal communication.
38
all significantly greater (a < 0.05) than of those fed
sediment from the more disturbed Muddy River site.
Paraleptophlebia spp. larvae, when provided
substrates of particle size ranges 53-125 urn and 125-250
urn from stream sites on Mount St. Helens, exhibited a loss
of mass on all treatments regardless of particle size or
presumed nutritional quality of the food resource (Table
11, Experiment 7).
Animals provided substrates (in the
range 125-250 urn) from Yellowjacket Creek, Elk Creek, and
Middle Clearwater Creek lost significantly less body mass
(a < 0.01) than did those provided the same particle sizes
from the most affected site, Lake Creek.
Volcanic ash is primarily composed of glass (Fruchter
et al. 1980; Hooper et al. 1980) in which elements (e.g.,
P, K, Cu, Fe, Zn, and Mn) are either unavailable or
present in very low concentrations (Cook et al. 1980).
The abrasive nature of volcanic ash was probably
detrimental to these animals.
Ptychoptera townesi survive
in greater numbers and for considerably longer periods on
silica sand than they do on ash.
Mayf lies appear to be
even more sensitive to the volcanic substrate than are
ptychopterids.
Gersich and Brusven (1982) found that
aquatic invertebrates show considerable short-term (24 h)
tolerance to external ash accumulations.
Yet, as an
abrasive, ash has been found to be lethal to certain
insects (Cook et al. 1980).
39
Table 11.
Survival and growth (mean ± standard error)
of paraleptophiebia spp. on sediments from
progressively affected sites on Mount St.
Helens (Experiment 7).
Site
Substrate
particle size
range (urn)
Substrate Survival
organic
content (%)
Relative growth rate
(% body wt/d)
Yellowjacket
53-125
Creek
* 125-250
(least affected
3.4
1.5
100
-1.47 ± 0.26
Elk Creek
53-125
125-250
1.6
1.1
0
67
-1.27 t 0.34
Middle Clearwater 53-125
125- 250
0.7
0.7
100
-0.47
-0.64 ± 0.43
53-125
125-250
7.3
2.9
67
100
-1.19 ± 0.29
-2.44 * 0.69
Lake Creek
(most affected
*
*
C.p. Hawkins, persona]. communication.
0
33
40
Mouthparts
Scanning electron micrographs of the heads,
mandibles, and maxillae of Ptychoptera townesi and
Paraleptophlebia spp. are presented in Figure 2.
The
position of the false crane fly's mandibles and their
overall shape suggest that these structures are suitable
for scooping sediment and possibly for cleaning the hairs
of the labrum.
The mayfly's mandibles, however, have
closely fitting teeth and molar areas apparently able to
reduce material to particles of ingestible size.
The
numerous fine hairs of the maxillae of both genera appear
to be suited for collecting and retaining fine particulate
material.
These structures indicate, as do experimental
studies reported in later sections, that false crane fly
larvae may be not only adapted, but restricted to feeding
on FPOM, whereas the mayf lies may be capable of feeding on
both CPOM and FPOM.
Paraleptophlebia spp. were observed to shred leaf
disks prepared from leached red alder (Alnus rubra) leaves
(Figure 3a), whereas Ptychoptera townesi exhibited no such
capability.
Larvae of both the false crane fly and the
mayflies were found to ingest hydrolyzed filter paper
(method of Bãrlocher and Kendrick 1975).
The mayf lies
shredded numerous small particles from the substrate,
whereas the false crane flies ingested material loosened
from the paper surface.
41
Figure 2.
Scanning electron micrographs of the head
capsules of Ptychoptera townesi (a at 200x) and
Paraleptophiebia sp. (b at lOOx), and their
respective mandibles (c at 500x and e at l000x,
d at 200x). A maxilla of the mayfly is shown
in f (200x).
42
ri
Figure 2.
43
Figure 3. Photographs (a) of red alder leaf disks fed on
for 1 - 2 h by Paraleptophiebia spp. and (b) of
Ptychoptera townesi and Paraleptophiebia spp.
with feces (the false crane fly egests the
larger particles).
Scanning electron micrographs of the fecal pellets of Ptychoptera
townesi (c at 200x) and Paraleptophiebia spp.
(d at 500x), and respective sections from each
(e and f at 2000x).
44
L
H4i:
C
e
Figure 3.
f
45
Alimentary tracts
The alimentary tract of the false crane fly larva is
considerably more complex than that of either species of
mayflies (Figure 4).
It contains gastric ceca, which
increase the secretory and absorptive area of the midgut,
and a proventriculus, actually the anterior part (cardia)
of the ventriculus (Mahxnud-ulAineen 1969), with an
esophageal invagination.
In addition, the middle segment
of the anterior two of the five Malpighian tubules is a
modified saccular tube.
The gut tract of the mayfly is
essentially straight and extends the length of the body
(Figure 4).
The digestive systems of Paraleptophiebia
spp., as in most Ephemeroptera, are.characterized by a
relatively large midgutand numerous Malpighiari tubules
(Needham et al. 1935; Richards and Davies 1977).
The gut tract of Ptychoptera townesi is several times
longer than the animal's body length, whereas that of the
mayfly species extends only the length of the body.
This
may increase the time required for passage of material
through the gut of the false crane fly and, thereby,
provide more time for digestion and/or for digestion of
more material in a given period of time (Sibly 1981).
The proportion of hindgut volume to total gut volume
is much larger in Ptychoptera townesi than in
Paraleptophiebia spp. (Figure 4).
In the majority of
insects exauined by Meitz (1975), the midgut was the most
46
Figure 4.
Alimentary tracts of (left) Ptychoptera
townesi and (right) Paraleptophiebia sp. f =
foregut; gc = gastric ceca; h = hindgut; i =
ileum; is = lime sac; mt = Malpighian tubules;
o = esophagus; p = proventriculus; r = rectum;
s = salivary gland; v = ventriculus or midgut
(differentiated according to Wigglesworth
1972).
47
mt
Figure 4.
48
capacious of the three gut regions, in many cases larger
than the hindgut by a factor of ten.
for Paraleptophiebia spp.
This is true as well
Meitz (1975) found that these
proportions were reversed in the crane fly and in
megalopterans, although in Tipula abdominalis the hindgut
was only 2-3 times larger than the midgut.
The hindgut of
Ptychoptera townesi, although not ten times larger, is
more voluminous than the other two gut regions.
Not only
can the proportionately larger hindgut of Ptychoptera
townesi hold a larger store of substrate, but also it
Contains a relatively greater number of microorganisms of
probable importance.
Tipula abdominalis reared under
sterile conditions do not survive past the first larval
instar (M.J. Klug, personal communication), and isopod
larvae reared aseptically do not survive more than 30 days
(Ross! and Vitagliano-Tadini 1978).
Aquatic insects commonly harbor microbiota (Meitz
1975).
Qualitative observations by epifluorescence
microscopy indicate that microbes in the guts of both
Ptychoptera townesi and Paraleptophiebia spp. increase in
relative number along the alimentary tract from foregut to
hiridgut.
The types and sizes of microbes change from
those morphologically similar to substrate microbes in the
midgut (primarily cocci and short rodlike forms) to forms
ccrtonly found in invertebrate hindguts (e.g.,
spore-forming filamentous bacteria and rods).
Flagellated
49
protozoans inhabit the hindgut of Ptychoptera townesi.
The alkaline pH of the foregut and midgut of some
detritivores (e.g., Tipula abdominalis; Martin et al.
1980) provides conditions under which proteins complexed
with phenols or lignin might be released and then broken
down enzymatically.
Although a dark band (apparently of
amorphous deposited material) approximately 0.1 mm in
length was frequently observed around the anterior portion
of the hindgut of Ptychoptera townesi,
the gut tracts of
this species and Paraleptophiebia spp. are not discolored
in the same way as are those of invertebrates with gut
regions of high pH.
Further investigations using a pH
microelectrode showed that none of these animals has a
region of high pH along the digestive tract.
Food handling: consumption
Larvae of the false crane fly consume food substrates
more slowly, in time and per unit of body mass, than do
the mayflies, which are able to feed on coarse
particulates as well as FPOM.
Under the experimental
conditions provided, consumption rates (CR) and
consumption indices (CI) indicate that Ptychoptera townesi
consumed substantially less UPOM than Paraleptophiebia
spp. consumed leaf material (Table 12).
Consumption values for both genera, again, under the
experimental conditions provided, were lower than those
which have been determined for other deposit-feeders.
A
50
Table 12.
Consumption rate (CR), consumption index (CI),
and efficiency of conversion of ingested food
to body substance (Ed) (mean ± standard
deviation) for Ptychoptera townesi on UPOM and
Paraleptophiebia spp. on alder leaves.
Trophic index
Ptychoptera townesi
Paraleptophiebia app.
CR (m/d)
0.002 ± 0.001
0.060 ± 0.033
CI (mg/mg/d)
0.002 * 0.001
0.158 * 0.089
Ed
20.68
* 9.03
0.08
0.07
Si
consumption index determined for third and fourth instar
larvae of the chironomid Stictochironomus annulicrus (on
sediment 63 urn - 1 mm in diameter at 7°C) was 0.324 ±
0.029 mg/mgjd (R.H. King, personal communication).
Mayflies Tricorythodes minutus were found to ingest 3.8
times their body weight per day (Mccullough et al. 1979),
and Hexagenia limbata have the capacity to ingest over
100% body mass (dry) per day at
(Zimmerman and
10-25°c
Wissing 1980).
Observations by epifluorescence microscopy of animals
ingesting dyed substrates indicated that both Ptychoptera
townesi and Paraleptophiebia spp. sometimes do not feed.
Both exhibited variable ingestion rates.
False crane fly
larvae were found to ingest relatively uncolonized
particles of pignut hickory leaf litter at a slower rate
than that at which they ingested stream sediment
(unpublished data).
The rate of ingestion is dependent
partially on the available substrate.
Dermott (1981)
found that Hexagenia liinbata larvae daily ingest more
sandy sediment than they ingest organic matter (thereby
apparently compensating for the reduced nutritional value
of the sediment).
Ancylus fluviatilis (a grazer) arid
Planorbis contortus (a detritivore) have been found to
increase their rate of ingestion when food quality is
reduced (Calow 1975a).
Food intake may be reduced prior
to and after moulting, although the physiological factors
52
for this are not known (Bernays and Simpson 1982).
Only
data for animals that exhibited positive rates of growth
were used in the calculation of indices reported in Table
12.
Food handling: gut content passage time
Measurements of gut content passage times for both
Ptychoptera townesi and Paraleptophiebia spp. are
variable.
Determinations with dyed cellulose mixed with
Berry Creek sediment (less than 500 urn, at
10°c)
yielded values greater than 19 ri for Ptychoptera townesi
and less than 3 h for Paraleptophlebia spp.
The shorter
retention times recorded for the mayflies are similar to
those observed for other aquatic invertebrates.
For
example, Chironomus thumini have retention times of less
than 2 h (Baker and Bradnam 1976), and Gainmarus
pseudolimnaeus have retention times of 45-120 mm
(Bärlocher and Kendrick 1975).
Material remains in the mayflies' hindguts for a very
short period, observed to be less than 1 mm.
Thus,
little time is available for hindgut microbes to colonize
the mayflies' gut contents.
Observations by
epifluorescence microscopy of Paraleptophlebia spp. gut
contents indicate that they are not colonized by microbes
typically found in the hindgut.
Retention times of git
material in the hindgut of the false crane fly larvae are
comparatively long (hours).
Observations of gut contents
53
by epifluorescence microscopy indicate that particles in
Ptychoptera townesi hindguts are heavily colonized with
microbes typical of hindgut microflora, notably the
spore-forming filamentous bacteria.
Ptychoptera townesi
retain material in the gut in the absence of food input
longer, and pass material through the gut more slowly,
than do Paraleptophiebia spp.
The effect of such
retention on consumption rate is not known.
The timing of
feeding must be partially determined by the fullness of
the gut (Bernays and Simpson 1982).
The relatively long time of material passage through
the guts of false crane f1ies could allow the animals to
derive more nutrition from particles than they would if
the material passed through the gut more rapidly.
Assimilation could be even more effective if the animals
refluxed material from the hindgut through the ileum into
the midgut for digestion of the hindgut microbes which
colonize the particles.
The midguts of these animals
occasionally were observed to contain particles well
colonized by typical hindgut microbes, including bacterial
filaments and tufts of filaments.
These particles were
indistinguishable from those found in the hindgut.
This
may provide evidence of a capacity for ref luxing, but the
gut sections were not ligatured, so the presence of these
particles could reflect only experimental contamination.
Natural movement of the false crane flies (i.e.,
54
their ability to extend and contract the body as they
burrow into and through sediment) undoubtedly facilitates
movement, potentially selective, of gut contents.
In
addition, the gut contents of Ptychoptera townesi that
were allowed to feed (eight days,
10°c) on hydrolyzed
filter paper were found on dissection to consist of a
sediment-paper mixture.
This suggests that the larvae
mixed a portion of the previous gut contents (sediment)
with newly ingested material (filter paper).
Similarly,
when this species was allowed to feed on cation exchange
resin, the animals' foreguts generally remained full of
detritus, even though resin particles were mixed
throughout the contents of the midgut and hindgut.
Mixing
of material in the gut may serve several functions,
including facilitation of assimilation and of microbial
colonization of recently ingested material.
In addition to the mixing of gut contents with newly
ingested material, false crane fly larvae apparently
retain a portion of previously ingested material, which
might then be further digested and/or mixed with newly
ingested substrate.
Animals deprived of food for one
month were found on dissection to contain a "plug" of
substrate colonized by numerous microbes, including those
typical of the hindgut microflora.
This material was
located in the anterior loop portion of the hindgut.
Ptychoptera townesi ingest nonnutritious substrates
55
(relatively sterile wood particles), but pass these and
materials of low nutritional value (relatively uncolonized
pignut hickory leaf particles) through the gut at a slower
and more variable rate than that at which they pass
natural stream sediment.
In addition, dissections
indicated that false crane fly larvae do not ingest
particles of silica sand when that is the only substrate
provided.
Indeed, a greater percentage of these animals
survived on substrates such as sand as compared with wood
(unpublished data), this suggesting they may handle
periods of starvation (they survive at least a month in
water alone) better than they survive periods of ingesting
nutritionally poor substrates.
Of course, the animals
lose weight on these nutritionally poor substrates.
Although Calow (1975b, 1977) noted increased ingestion
rates when food quality was reduced, he reports that
Ancylus fluviatilis increase retention times when food is
scarce.
Blackfly larvae have been reported to increase
gut content retention time as they increase in size
(Wotton 1984).
Food handling: assimilation
Efficiencies of conversion of ingested food to body
substance (ECIs) were determined for Ptychoptera townesi
and Paraleptophiebia spp. feeding on the respective
substrates, UPOM and alder leaves, on which they exhibited
the highest relative.growth rates (Table 12).
56
Assimilation values measured for false crane fly larvae
were unexpectedly high.
Only animals with positive growth
rates were used in these determinations.
Animals used for
these analyses were relatively small (Table 1), second
instar larvae.
Early instar Ptychoptera townesi exhibit
rapid growth, and this would tend to favor higher
efficiencies.
By comparison, efficiencies measured for
Paraleptophiebia spp. were low and similar to those
measured for other detritivores.
As was noted earlier, the relative growth rates of
the false crane flies and the mayflies generally differ
markedly on UPOM and leaf litter, and possibly reflect
acquisition and assimilation capabilities.
The
nutritional quality of conditioned leaf litter is
generally relatively high, whereas that of UPOM is more
variable depending on the process by which it is formed
and its stage of decomposition (Cummins and Kiug 1979).
Measured efficiencies of conversion of ingested food
to body substance of aquatic and terrestrial arthropods
feeding on wood, litter, and detritus generally
approximate 1% (Mattson 1980).
to be variable.
Yet, assimilation is known
As would be expected, ecological
efficiencies of invertebrates vary with conditions, e.g.,
food quantity and quality (Bàrlocher and Kendrick 1975;
Mattson 1980) and age (Calow 1975a).
The results
presented here cannot have been independent of these and
57
other factors.
Food handling: egestion
Mean and relative rates of egestion were determined
from pooled estimates of two trials made within a
three-week period on animals fed Berry Creek sediment less
than 500 urn at 4, 10, and 18°C (Table 13).
maintained at 18°C survived.
No animals
Whereas Paraleptophiebia
spp. egested nearly twice as much per mg dry mass animal
at 10°C as they did at 4°C, no apparent
temperature effect on egestion is shown for Ptychoptera
townesi.
Many dipterans, including Ptychoptera townesi,
enter a prepupal period of reduced activity, and animals
used in late June analyses may have been nearing pupation.
During this investigation, Ptychoptera townesi were
observed to completely empty their gut tracts of food
material up to a week prior to pupating.
Flargrave (1972) noted that Eyalella azteca fecal
production increases linearly with temperature between
5°C and 20°C.
The rate of defecation by
oligochaetes is also affected by temperature, but the
effect varies from species to species (Appleby and
Brinkhurst 1970).
Ptychoptera townesi egestion rates
(determined on a per animal rather than a per dry mass
basis) were variable, even when food was abundant (Figure
5).
Amounts of material egested by separate groups of
fourth-instar larvae after feeding on Berry Creek detritus
58
Table 13.
Daily (mg/d) and relative (mg/mg/d) rates of
egestion (mean ± standard error) by Ptychopt8ra townei and paraleptophiebia spp. at
4 C and 10 C.
Temperature
Ptychoptera townesi
Egestion rate
Daily
Relative
(°C)
n
40
100 C
Paraleptophiebia spp.
(mg/d)
(xng/mg/d)
Egestion rate
Relative
ily
(mg/d)
n
(ing/mg/d)
17
0.15 ± .02
0.03 ± .01
5
0.04 ± .01
0.07 ± .02
22
0.17 ± .03
0.04 j .01
26
0.07 ± .01
0.12 ± .02
59
Figure 5.
Egestion rates (mg/animal/h) by Ptychoptera
townesi.
(a) Food available continuously,
(b) animals removed from substrate prior to
measurement, (c) Food available initially but
animals removed from substrate (arrow) after a
period of feeding.
-C
E
C
E
0
0
20
50
40
30
60
-C
E
C
-E
0
20
10
40
30
0
0
OO4
(c)
I
It
\i
0.03-
C
o
'
.c
O.O2-
'WV"
E
['I'll
0
Figure 5.
10
20
30
40
5
20
40
TIME (h)
60
80
130
I
61
or on leached pignut hickory particles (relatively
unconditioned and ground, 53-500 urn) for 11 days at
10°C differed greatly (0.312 and 0.042 mg dry
wt/animal, respectively).
This also supports the
contention that Ptychoptera townesi discriminate among
substrates differing in food quality.
Ingestion rates and
gut content passage times of Ptychoptera townesi on
particles of relatively uncolonized hickory were reduced
from those measured on stream detritus.
The animals not
only pass this material through the gut tract more slowly,
but also feed on it and egest it more slowly than they do
stream detritus.
These substrates differ in numerous
qualitative parameters, including organic content,
respiration, C:N ratio, and texture.
Recycling of fecal material
Scanning electron micrographs of compacted fecal
pellets from Ptychoptera townesi and more loosely
aggregated feces of Paraleptophiebia sp. are provided in
Figures 3c and 3d.
Section enlargements to the same
relative magnification (2000x) of these animals' feces
(Figures 3e and 3f) further indicate the more compacted
nature of the false crane fly's fecal pellets.
A
photograph (Figure 3b) of Ptychoptera townesi and
Paraleptophiebia sp. with their fecal material .shows the
relative size of particles egested by the false crane fly
(larger particles), and those egested by the mayfly.
The
62
animals that apparently are restricted to feeding on small
particles egest feces that are considerably larger than
the material originally ingested, whereas the animals
capable of feeding on relatively large substrates egest
material considerably smaller.
Ptychoptera townesi fecal pellets are generally
extruded from the peritrophic membrane during egestion.
As noted, epifluorescence and light microscopy revealed
that these pellets are heavily colonized by bacteria and
associated protozoans.
This is in contrast with reports
of invertebrates egesting pellets that are almost devoid
of bacteria (Fenchel 1972; Lautenschlager et al. 1978).
Pellets of animals egesting relatively sterile particles,
however, are generally covered with a peritrophic
membrane.
It is the membrane and not the fecal material
that is relatively microbe free.
Some deposit-feeding animals, e.g., Hydrobia ulvae,
are able to ingest and partially assimilate their own
feces, which are rapidly colonized by microbes, this
increasing the relative nitrogen content of egested
material (Newell 1965).
Although the extent of microbial
input is debatable (Rice 1982), microbial colonization
might be beneficial to an animal able to retain food
particles in its gut tract for long periods of time and
thereby derive a large portion of the potential
nutritional value.
63
In order to determine whether or not Ptychoptera
townesi can obtain nutrition by coprophagy, larvae were
provided freshly egested fecal material from their own
species feeding on UPOM (Experiment 8, Table 14).
These
animals lost weight on both the alder leaves and the
richly colonized fecal material.
Comparison with growth
rates on UPOM suggests Ptychoptera townesi are not capable
of reingesting material that has passed through their
alimentary tracts.
Their cylindrically shaped fecal
pellets are greater than 125 urn in diameter and of
variable but longer length.
Ptychoptera townesi
invariably lose weight when presented substrates in this
particle size range, this suggesting that such particles
are too large for ingestion.
Moreover, the fecal pellets
are approximately the same size as the animal's head
capsule (Figure 3b).
When maintained with Ptychoptera
townesi larvae at 10°C in 53 urn-filtered stream water,
the fecal pellets remain intact, for at least one month.
Thus, Ptychoptera townesi are apparently unable to
dismantle these pellets.
In contrast, Paraleptophlebia
spp. reduce them to fine particles in less than one hour.
Compaction of fecal material may prevent reingestion
of substrate from which nutrients have been largely
absorbed by Ptychoptera townesi, may provide substrate of
suitable size for a co-occurring species, and probably
serves other functions.
In some deposit-feeders, fecal
64
Table 14.
Survival and growth (mean ± standard error)
of Ptychoptera townesi and Paraleptophiebia
spp. on UPOM and alder leaves from Berry Creek,
and on feces collected from Ptychoptera
townesi feeding on UPOM (Experiment 8).
Ptychoptera townesi
Substrate
Substrate
organic
content
Survival
(%)
Paraleptophlebia app.
Relative
growth rate
(% body wt/d)
Survival
(%)
Relative
growth rate
(% body wt/d)
46
2.08 ± 1.23
(%)
Alder
leaves
87.9
90
-1.03 ± 0.05
feces
50.0
85
-1.27 ± 0.06
OPOM +
alder
leaves
46.5
80
-0.05 ± 0.27
Ptychoptera
townesi
ND
39
2.69 ± 0.72
65
material has been found to support higher growth rates
than does nonfecal material (Ward and Cummins 1979;
Shepard and Minshall 1981).
Effects of ingestion of feces
by co-occurring species have been documented for
oligochaetes (Brinkhurst et al. 1972), as has enhancement
of collector growth in the presence of particle-producing
shredders (Short and Maslin 1977).
The coprophagic ability of Paraleptophiebia spp. was
not examined.
Paraleptophiebia spp. exhibit no
significant differences in growth, whether feeding on
alder leaves, alder leaves with shredders (Zapada sp. and
Lepidostoma sp.) present, or Holorusia sp. feces
(Experiment 9, Table 15).
Ptychoptera townesi, on the
other hand, grow at a significantly (a < 0.01) greater
rate on Holorusia sp. feces (53-500 urn) than on alder
leaves (Table 15).
Thus, Ptychoptera townesi appear not
to avoid fecal material in general, feces of other species
probably containing nutrients unavailable in their own.
Growth rates were intermediate when Ptychoptera townesi
were fed alder leaves with shredders present (Table 15).
The rate of fecal production by shredders present may have
been inadequate to support the rate of Ptychoptera townesi
growth measured on shredder feces alone.
In a similar study (Experiment 10, Table 16),
Ptychoptera townesi lost mass on fecal material from
shredders (Holorusia sp.) at a rate not significantly
Table 15.
Survival and growth (mean ± standard error) of
Ptychoptera townesi and Paraleptophiebia spp.
on alder leaves, alder leaves with shredders
(Lepidostoma sp. and Zapada sp.), and feces
from shredders (Holorusia sp.) which were fed
alder leaves (Experiment 9).
*
Substrate
Ptychoptera townesi
Survival Relative growth
rate (% body wt/d)
(%)
Paraleptophlebia spp.
Survival Relative growth
rate (% body wt/d)
(%)
Alder leaves
92
-0.58
0.16
31
0.71 ± 0.76
Alder leaves with
shredders present
67
-0.11 ± 0.08
37
0.79 ± 0.65
75
0.36 ± 0.11
31
0.48
Feces (53-500 urn)
from shredders fed
alder leaves
*
Organic content, 78-79%.
67
Table 16.
Survival and growth
Ptychoptera townesi
on alder leaves and
(Holorusia sp.) fed
(Experiment 10).
(mean ± standard error) of
and Paraleptophiebia spp.
on feces from shredders
alder leaves
Ptychoptera townesi
Paraleptophlebia spp.
*
Substrate
Survival Relative growth Survival Relative growth
rate (% body wt/d)
(%)
rate (% body wt/d)
(%)
Alder leaves
50
-0.90 ± 0.56
67
1.88 * 0.92
100
-0.84 ± 0.30
50
0.63 ± 0.53
Feces (250-500 urn)
from shredders
fed alder leaves
*
Organic content, 88-94%.
different from that which occurred on alder leaves.
As in
Experiment 9 (Table 15), Paraleptophiebia spp. grew well
(no significant difference) on both alder leaves and
Holorusia sp. feces.
Life History
Paraleptophiebia spp. in general are univoltine with
either a spring or fall emergence (Table 17).
Paraleptophiebia temporalis have a single generation per
year (Edmunds et al. 1976).
In Oak Creek, this species
passes the summer in the egg stage, hatches in the fall,
and emerges from April to June (Lehinkuhl and Anderson
The life cycle of Paraleptophiebia gregalis is
1971).
similar to that of Paraleptophlebia teinporalis.
Kraft
(1964) noted a second cohort of Paraleptophlebia heteronea
(= P. teinporalis; Lehmkuhl and Anderson 1971) in Berry
Creek in the fall and attributed it to temperatures
favorable for emergence during both periods.
townesi
Ptychoptera
also have a univoltine life cycle in Berry Creek,
but it is of longer duration than that of Paraleptophiebia
spp. and includes an extended summer emergence (Table 17).
The average fecundities of Ptychoptera and
Paraleptophiebia are similar, and both genera reportedly
oviposit at the water surface (Table 17).
In Berry Creek,
the false crane flies lay eggs in late summer (see also
Kraft 1964), at which time they undergo a brief
Table 17.
Information concerning voltinism and emergence,
oviposition, and fecundity of the genera
Ptychoptera and paraleptophiebia.
Ptychoptera spp.
Reference
Paraleptophlebia spp.
Reference
Voltiriisxa and Emergence:
Uru.voltine
-
extended, May-July
spring arid summer
Bivoltine
MultivOltine
Univoltine
9
1,7,?
5
"expanded'
Adults emerge
1
Adults emerge from water
surface
15,?
laid, 554
spring and fall
7,8,11,
1.2,13,?
2
pupae move from water to
moist ground
Oviposition:
In sphagnum at water surface
Fecundity:
Average number of eggs
-
13
from water surface
6,11
3
At water surface
11
2
Average number of eggs
in subimagoes, 264-1160
4,10
1. Miall 1895; 2. Topsent 1914-16; 3. Rogers 1933; 4. Ide 1940; 5.
Rogers 1942; 6. Leonard and Leonard 1962; 7. Kraft 1964; 8. L.ehmkuhl
1969; 9. Modkinson 1973; 10. CU.f ford and Boerger 1974 11. Edmurids
et al. 1976; 12. Sliapas and Hilserthoff 1976; 13. Corkum 1978; 1.4.
arTs and Carlson 1978; 15. Anderson and wallace 1984; P. present study.
70
developmental period.
Lehmkuhl and Anderson (1971) state
that most species of Paraleptophlebia in Oak Creek lay
their eggs in the fall and overwinter as eggs; however,
Paraleptophlebia temporalis and Paraleptophiebia gregalis
lay their eggs in the spring in Oak Creek.
Ptychoptera townesi have a holometabolous life
cycle,
Paraleptophiebia spp., a hemimetabolous cycle.
Ptychoptera townesi generally increase in individual mass
from late July/early August -- when dry masses range from
0.08 ± 0.02 (n = 53) to 0.17 ± 0.06 (n = 72) mg -- until
May/June -- when masses range from 4.23 ± 0.94 (n = 49) to
5.34 ± 1.44 (n = 76) mg.
Growth of these animals is
particularly rapid during early larval instars.
This
development coincides with increasing water temperature
during the late summer months.
Maximum growth rates in
related tipulids have been found to be associated with
rapid increases in temperature (Laughlin 1967) and/or
seasonal increases in food abundance (Pritchard 1978).
Individual masses of Paraleptophlebia spp. are high
in the May - June period (e.g., from 0.75 ± 0.35 [n = 48]
to 0.83 ± 0.34 [n = 50]) and again in the fall (e.g., 0.58
± 0.14 [n = 59] in October).
The number of instars for a
particular mayfly species may be variable (Brittain 1982).
And temperature, food quality, and other factors may be
expec.ted to affect growth and development of stream
invertebrates (Anderson and Cuminins 1979; Cummins and Klug
71
1979).
False crane fly and inayfly adults were collected
in emergence traps shortly after their respective periods
of maximum individual mass.
Paraleptophiebia spp. larvae range in organic
content from 70% of dry mass to greater than 95%.
higher than larvae of Ptychoptera townesi,
This is
which range
from 55% to 86% in organic content throughout the year.
The organic content of false crane fly pupae ranges from
82% to 86%.
No apparent trend in the organic content of
either mayfly or false crane fly larvae by season or by
stage of development was found.
Summary of Trophic and Habitat Requirements and Life
Histories
An animal's trophic requirements must be met in a
manner that is in accord with habitat and life history
requirements.
In this study, the deposit-feeding
organisms Ptychoptera townesi and Paraleptophiebia spp.
were found to differ in their life cycles and habitats as
well as in their utilization of detrital material.
False
crane fly larvae are abundant in a heavily sedimented,
flow-controlled stream channel segment, where particles
less than 250 urn in diameter have accumulated.
They are
rare both upstream and downstream from this stream
segment.
In contrast, Paraleptophiebia spp. are abundant
throughout the stream channel.
These genera differ in
relative distribution and mobility, duration and timing of
72
life cycle stages, and time of emergence.
The mayfly
larvae inhabit erosional habitats initially, but may move
to backwater areas as they mature.
quite mobile.
in addition, they are
Larvae of the false crane fly are rather
sluggish and inhabit depositional areas of the channel.
Both genera apparently emerge from the water surface, the
holornetabolous species in summer, the hemimetabolous
species in the spring and sometimes in the fall.
The
mayf lies in general spend the summer in the egg stage and
hatch in fall or winter. The eggs of the dipteran undergo
a brief developmental period prior to hatching in late
summer.
Ptychoptera townesi and Paraleptophiebia spp. differ
greatly in food acquisition and assimilation.
Both genera
are capable of altering the particle size of material on
which they feed.
Larval mayflies are able to feed and
grow on a variety of resource sizes and types (FPOM,
leaves, and periphyton).
False crane fly larvae are
restricted in feeding to FPOM less than 250 urn in
diameter, particularly from 0.45 to 53 urn.
Morphological,
physiological, and behavioral differences between these
genera are indicative of differences in feeding
capability.
Ptychoptera townesi larvae are apparently
able to adjust the period of retention of material in the
gut tract according to the nutritional quality of the food
resource, thereby allowing for further digestion and
73
coonization by hindgut microbes.
In addition, fecal
material is egested discontinuously and is of considerably
larger size than material ingested.
large for reirigestion.
It is probably too
The mayfly larvae egest relatively
small particles regardless of the original size of the
substrate.
Both organisms appear to grow on diets of some
kinds of fecal material of ingestible size.
In general, the pattern exhibited by Ptychoptera
townesi involves slow handling of relatively small volumes
of food which pass, probably only once, through an
elaborate alimentary tract.
Paraleptophiebia spp. rapidly
process and partially recycle large amounts of material
through a relatively simple alimentary tract.
Similar
tendencies were noted by Mattson (1980) for herbivores
feeding on a recalcitrant resource.
74
DISCUSSION
The quantity and quality of particle substrates
available to deposit-feeding invertebrates are important
in understanding macroinvertebrate distribution and
density (Rabeni and Minshall 1977; Brennan et al. 1978;
McLachlan et al. 1978; Walentowicz and McLachlan 1980).
Yet the singular view that members of the deposit-feeder
guild select particles on the basis of size and strip
microbes from particles may limit attempts to understand
generally the role of deposit-feeding organisms in stream
communities.
Members of this guild may obtain energy and
materials from detritus directly, indirectly (e.g.,
mediated by microbes)(Saunders 1980), or in both ways.
The relative importance of particle substrate, microbes,
and adsorbed or dissolved organic molecules in the
nutrition of detritivores continues to be debated (Table
18).
Further, and even though a variety of "measures" of
food quality are in common use (Table 19), understanding
of what entails "food quality" to organisms ingesting
detrital substrates is lacking.
A more general, unifying
perspective is needed.
Many studies reporting selective feeding are unclear
as to the basis for the stated selection.
Support for
statements on selection may range from an unknown basis
(Self and Jumars 1978), to emphasis on food quality,
75
Table 18.
Basis
Potential bases for detritivore nutrition.
Reasoning
PARTICLE SUBSTRATE:
Sheer quantity
References
Cammen et al. 1978; Levjnton 1979
Not enough microbes
in number, biomass, or
nutrient content
Baker and Bradnam 1976; Cammen et
al. 1978; Tunnicliffe and Risk 1977;
flndlay et al. 1984
Easily digested portions
Lopez et al. 1977
Nitrogen-rich portions
TenOre 1977; LevintOrt and Bianchi
1981
Benthic diatoms may be
locally important
Johannes and Satomi 1966; Fenchel
1969
ATTACHED, ASSOCIATED, AND INTERSTITUAL MICROBES:
Live on bacteria alone
Fredeen 1964
Only microbes are
digested
Hargrave 1970; Marchant and Hynes
Use bacterial epigrowth
Newell 1965; Fenchel 1970; Lopez
and Levinton 1978; Rounic}c and
Winterbourn 1983
1981
Bacteria are major source Newell 1965, 1970; Hargrave 1970;
FenChel 1970
Use microbes attached to
algae
Smyly and Collins 1975
Use epilithic detritus
through bacteria
Madsen 1972; Calow 1975c
Microbes provide more
complete nitrogen or
growth factors
Baker and Bradnam 1976;
Bàrlocher and Kendrick 1973
Directly or indirectly
(substrate alteration)
Newell 1965; Fenchel 1970; Wavre
and Brinkhurst 1971; Hylleberg
Kristensen 1972; Berrie 1976;
Yingst 1976; Lopez et al. 1977;
Rossi and Fano 1979; Cammen 1980
ADSORBED ORGANIC MOLECULES AND DISSOLVED SUBSTANCES:
Quantitatively
Krogh 1939
unimportant
Invertebrates other than
Arthropoda
Adams and Angelovic 1970; Stephens
and Schineke 1961; Sepers
1977; Stephens 1982
Ingest colloids and
surface film
Wotton 1976, 1982
Organic layers on stones,
nutritious, even with
Madsen 1972; Iversen and Madsen
little or no algae
1978; Rounick and Winterbourn 1983
76
Table 19.
Commonly used measures of food quality.
Measure
References
Protein
Lowry at al. 1951; Kaushik and Hynes 1971; Bowen 1979;
Rice 1982
Amino acids
Johannes at al. 1969
Organic content
King 1978; Ward and Cummins 1979; Mattingly et al. 1981
Organic carbon
Cammen at al. 1978; Cammen 1980
CHN
McMahon at al. 1974; Iiowarth 1977
Texture
Meadows 1964a; Lopez and Levinton 1978
Cellulose, lignin
Suberkropp and Klug 1976
Microbial biomass
Suberkropp and Klug 1976; Geesey et al. 1978; Perkins
and Kaplan 1978; Ward and Cummins l97; Porter and Feig
1980
Microbial activity Gilsori 1963; Hanson and Wiebe 1977; Ward and Cummins 1979
Stage of
decomposition
Tenore 1977; Tenore and Hanson 1980
Source
Tenore 1977
Fatty acids
Prins 1982; Hanson 1983
Chlorophyll
Geesey at al. 1978
Particle size
distribution
McLachlan et al. 1978; Walentowicz and McLachlan 1980
Unattached vs
attached microbes
Meadows 1965
Macroinvertebrate
relative growth
rate
Cummins and Kiug 1979; Mattingly et al. 1981
77
particle size, energy content, organic film (references
provided in Table 20), to digestive capability (Fredeen
1964; Chua and Brinkhurst 1973; Davies 1975; Baker and
Bradnam 1976), to habitat and behavior (Wieser 1956;
Becker 1958; Egglishaw 1964; Eriksen 1964; Jonasson 1972;
McLachlan 1977), or to various combinations of these (Chua
and Brinkhurst 1973; Wallace 1975; McLachlan 1977).
Moreover, selection on the basis of particle size or on
the basis of food quality refers to only one of numerous
possible selective processes, including acquisition or
ingestion.
Deposit-feeders may be specialized or
"selective" in many ways, all of which may influence their
survival, growth, and reproduction.
For example, animals
may not only selectively ingest a particular particle size
or type, but also selectively assimilate portions of this
material by such means as differential enzymatic
capabilities.
Or animals may selectively ingest
different resources, e.g., suspended or deposited
particulate organic material, by changing behavior or
habitat on a seasonal or other basis (MeLachian 1977;
Taghon et al. 1980).
Thus, one basis for selection does
not necessarily preclude others.
Processes involved in feeding are interrelated and
affect one another.
Gut content passage rates and gut
emptying may affect rates of ingestion, as may
environmental factors (Bernays and Simpson 1982).
78
Table 20.
Options of detritivores feeding on a
nutritionally poor resource.
References
Options
*
Alteration of ingestion rate
Cummins and Kiug 1979; Taghon 1981
Alteration of gut passage time
Calow 1975b, 1977
*
Alteration of digestive
capability or absorption rate
Fredeen 1964; Chua and Brinkhurst
1973; Davies 1975; Baker and
Bradnam 1976
*
Gut tract morphology
Vernberg and Vernberg 1970
Enzyme capabilities
Bjarnov 1972; Bärlocher and
Kendrick 1973; Monk 1976; Cuminins
and Kiug 1979; Martin et al. 1980;
Bärlocher 1982
p1 considerations
Berenbauni 1980; Martin et al. 1980
*
Efficiency of conversion
of ingested food to body
Cummins and Klug 1979
Prolong development
Anderson and Cummins 1979
*
Endo/ ectosymbionts
Buchner 1965; Meitz 1975; Klug and
Kotarski 1980; Cummins and Klug
1979
Occasional carnivory
Anderson 1976
*
Spatial or temporal
separation
Wieser 1956; Becker 1958; Cummins
1964; Egglishaw 1964; Eriksen 1964;
Kraft 1964; Jonasson 1972; Mackay
and Kalff 1973; Howard 1975;
McLachlan 1977; Pereira 1981;
Cummins and Klug 1979; Vannote and
Sweeney 1980
*
Mobility
Levinton 1972; Br1ocher 1982
Coprophagy
Newell 1965
*
Increase in body size
Wilson 1976; Mattson 1980
*
Alternate food sources
Bärlocher 1982
Differential ingestion on
the basis of the following:
*
particle size
Wieser 1956; Meadows 1964b; Ciance
1970; Fenchel et al. 1975; Rees 1975;
Wallace 1975; Wotton 1977;. Taghon
1982
organic film
Meadows 1964a; Gray 1966; Taghon
1982
*
nutritious particles
Davies 1975: Hylleberg and Gallucci
1975; Zimmerman at al. 1975; Bolton
and Phillipson 1'76
energy content
Carefoot 1973
.
Related to this investigation of Ptychoptera townesi and Paraleptophlebia spp.
79
Selective ingestion and specialization in digestive
capabilities allow resource segregation in mixed species
colonies of tubificids (Chua and Brinkhurst 1973).
Taghon
(1980) suggests that disparate trends found in trophic
studies may be the result of various uncontrolled
variables (e.g., substrate texture) that prevent animals
from ranking their food items along a one-dimensional axis
(sensu Gray 1979) of food quality.
Much of the literature on foraging theory cannot be
interpreted for the deposit-feeder guild, because these
organisms are "bulk feeders" (i.e., they feed on masses of
particles rather th n ingesting them individually).
Fauchald and Jumars (1979) distinguish between
"macrophages," that handle food items singly and
"microphages," that handle food items in mass without
manipulating them individually.
Most aquatic
deposit-feeders are inicrophages and regularly ingest
unsuitable food items.
Much particle-size selectivity is
a direct consequence of the mechanics of operation of the
feeding appendages.
Taghon (1981) suggests that mobile
microphages can select among patches of food for those of
highest quality, whereas sessile microphages are limited
not only in selective abilities among food items but also
in ability to find new food patches.
He notes that
sessile organisms may vary gut content passage times and
ingestion rates as a function of food quality in order to
maximize the net rate of energy intake.
In line with this view, Paraleptophiebia spp., the
more mobile species, might be expected to select leaf
substrates over FPOM (the leaves produce more growth),
whereas Ptychoptera townesi, a relatively sluggish,
burrowing species, may alter ingestion rate and/or gut
content passage time according to substrate quality.
Bàrlocher (1982) argued that a shredder specialized on
digesting leaves with rich microbial growth and high
enzymatic activity must be highly mobile and/or have
access to alternative food sources.
He found this to be
so for most Gamniarus species, facultative shredders, but
not for Tipula abdominalis, obligate shredders.
Results
of the present investigation indicate that Ptychoptera
townesi are constrained morphologically to feeding on
relatively small particles.
Yet the experimental findings
and the behavior of the deposit-feeding organisms
Ptychoptera townesi and Paraleptophlebia spp. can be
interpreted in ways other than as being primarily related
to particle-size selection (i.e., independent of food
quality).
The behavioral repertoire of holometabolous
larvae in particular is often extremely modified for the
ingestion of food (Truman and Riddiford 1974).
Increased sedimentation and changes in flow and
temperature regimes may affect stream benthos by
physically, chemically, and microbiologically altering the
81
food resource and habitat (e.g., Paerl and Goldman 1972;
Moring 1975; Ringler and Hall 1975; Malmqvist et al.
1978).
Alteration of the flow regime of the experimental
portion of the Berry Creek channel has resulted in
environmental changes -- in part related to particle size
-- favoring Ptychoptera townesi.
To attribute observed
changes in the distribution and abundance of this species
directly to particle size, quality, or amount, however, is
not possible.
Ptychoptera townesi larvae reduce ingestion
and egestion rates and gut content passage times on
substrates of reduced food quality (in terms of microbial
colonization and texture).
This and any number of other
factors and responses are no doubt involved in determining
the distribution and abundance of aquatic invertebrates.
Food quality indirectly may affect the sensitivity of
aquatic invertebrates to various toxicants (Winner et al.
1977; Buikema and Benfield 1979; Buikema et al. 1980).
Food quality, food quantity, and temperature may affect
voltinism, growth rate, and size at maturity (Anderson and
Cummins 1979).
And effects that may appear to be
relatively minor in the short term may lead to eventual
population extinction (Lehmkuhl 1979).
undeniably affect organisms.
System alterations
But the particular response
of a deposit-feeding organism to such alteration is not
fully predictable.
The potential adaptive capacity of animals utilizing
82
detrital resources is immense (e.g., Table 20).
Differential responses found in studies reported here are,
therefore, hardly surprising.
Such capacity is neglected
when primary- emphasis is placed on the processing of
stream detritus.
Even if the particular role of these
organisms in detrital processing could be so simply
delineated and defined (it cannot), this focus obscures
other roles played by these organisms in aquatic systems.
Some deposit-feeding organisms no doubt digest microbes
off particles, which are recolonized on egestion and
become increasingly recalcitrant.
But assuming that this
is the major role of these organisms confines thinking
about the deposit-feeder guild to a link in a chain of
detrital processing from large to small, to relatively
more refractory substrates, until the material has been
mineralized.
Habitat, life history, and trophic relations all
interact to determine species distributions and
abundances.
Feeding activities of deposit-feeding
organisms no doubt result in modifications of substrate
particle size and quality that may make substrates more
(or less) suitable for particular species, given their
individual capacities and requirements.
Some members of
this guild switch over into other modes of feeding (e.g.,
shredding, suspension-feeding) and other habitats with
change in life stage (e.g., Edmunds et al. 1976) or
83
environmental conditions (e.g., McLachlan 1977; Tenore et
al. -1980).
In this regard, the deposit-feeder guild might
be viewed as one that integrates.
These animals with
their various capacities are constantly affecting and
being affected by relationships with other
deposit-feeders, other guilds, and their nutritional
resources and habitats.
This broader reasoning allows for further
understanding of the roles of deposit-feeding organisms
within the context of stream systems.
The concept of
community as having structure and organization and
developing over time (Warren et al. 1979) may facilitate
understanding of the nature of stream communities.
Deposit-feeding organisms clearly affect both the
structure and the development of the community as a whole
-- and they do so primarily through their response to and
effects on particulate and other substrates.
The effects
of particular deposit-feeders no doubt change in time with
community development and concomitant changes in structure
and organization.
More particularly, the role of some
deposit-feeding organisms as integrators ('linkers"
according to Wevers 1983) in stream community organization
and development helps to provide coherence to the stream
community.
Understanding the role of deposit-feeding organisms
-- as integrators or otherwise -- is critical to
84
understanding stream systems generally, because they are
so ubiquitous.
Much can be gained from the study of these
animals if we refuse to reduce them to a common
denominator of detrital processors.
Deposit-feeding
organisms modify the substrate -- undoubtedly
qualitatively as well as quantitatively -- in ways not
taken into account in a particle reduction and bacteria
stripping mode of thinking.
The integral nature of the
relationships between these organisms, the stream
environment, and their interactions within this context
should be recognized.
In such a context, studies such as
those presented here may further much needed understanding
of stream communities as being comprised of
interdependent, developing subsystems.
85
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