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

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 ofPhilosophy in

Fisheries and Wildlife presented onJuly 2, 1985 Title: Trophc and Habitat Requirements of Two Deposit-Feedi Stream Inverebrates, Ptychóptera townesi (Diptera) and paraleptophibia spp. (Ehemerotera)

Abstract approved; Redacted for privacy Chailes E. Warren

Ptychoptera townesi (false crane fly, Diptera)occur in

high densities in an experimentalstream section that has not

been allowed to exceed bankfull flow formore than two decades,

but are quite rare in areas both upstream anddownstream from this section. By contrast, ParaleptophJ.ebia spp. (mayfly,

Epherneroptera) are relatively abundant throughoutthe channel. Paraleptophiebia spp. are able to feed andgrow on a variety of

resource types, whereas Ptychoptera townesiare restricted to

feeding on fine particulate organicmatter (FPOM) less than 250 urn in diameter, particularly 0.45-53 urn. Morphological and behavioral differences between thesegenera are indicative of differences in feeding capability.

These genera also differ in responseto refractory food resources. The alimentary tract of the dipteran is considerably more differentiated than the simple straight tubegut 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 Paraleptophlebiaspp.(2-3 h) on these respective food resources. 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 ata 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 9 Organisms 9 Primary Collection Sites 9 General Experimental Design 11 Macroinvertebrate and Substrate Analyses 13 Procedure for tracking animals and determination of mass 13 Growth rate determination 14 Consumption and efficiency indices 15 Gut content passage time 16 Egestion 17 Substrate particle size distribution 18 Organic content 18 Microscope studies 18 Statistical Analyses 19

RESULTS AND INTERPRETATION 21 Habitat Requirements 21 Berry Creek substrate 21 Relative mobility of animals 22 Relative animal distribution 23 Trophic Requirements 28 Resource type and particle size 28 Effects of environmental alteration 34 Mouthparts 40 Alimentary tracts 45 Food handling: consumption 49 Food handling: gut content passage time 52 Food handling: assimilation 55 Food handling: egestion 57 Recycling of fecal material 61 Life History 68 Summary of Trophic and Habitat Requirements and Life Histories 71

DISCUSSION 74

LITERATURE CITED 85 LIST OF FIGURES

igure

1. Interrelationships among morphological, behavioral, and physiological constraints on survival and growth of deposit-feeding organisms. 7

2. 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). 41

3. Photographs (a) of red alder leaf disks fed on for 1 - 2 h by Paraleptophiebia spp. and (b) of Ptychoptera towrlesi and Paralepto- phlebia 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

4. 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

5. 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 Page

1. Details of experimental design of individual trophic investigations, and estimated mean initial dry mass (± standard deviation) of experimental animals. 12

2. Size distribution and organic content of particles less than 1tan 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

3. Mean percentage organic content (± standard deviation) of substrates collected from habitat types within the flow-controlled section of Berry Creek (Benton County, Oregon). 23

4. General habitatsof larvae of the genus Ptychoptera (tenspecies in North America) and of the genusParaleptophlebia (33 species in NorthAmerica). 26

5. Comparative survival and growth (mean ± standard error) of Ptychoptera townesi and Paraleptophiebia spp. on coarse and fine ?articulate organic matter (Experiment 1). 29

6. Survival and growth (mean) of Ptychoptera townesi (± standard deviation) and Paralep- tophlebia spp.(± standard error) on FPOM size fractions of ground, leached alder particlAs (Experiment 2). 32

7. Relative growth rates (mean ± standard error) and survival of Paraleptophlebia spp. on particle size fractions of sediment from Oak Creek (Experiment 3). 33

8. 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.) Page

9. 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 10. Survival and growth (mean ± standard error) of Ptychoptera townesi on sediments collected from variously disturbed sites on Mount St. Helens (Experiment 6). 37 11. Survival and growth (mean ± standard error) of Paraleptophlebia spp. on sediments from progressively affected sites on Mount St. Helens (Experiment 7). 39 12. 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 Paraleptophiebiaspp. on alder leaves. 50

13. 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

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). 64

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). 66 16. 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

17. Information concerningvoltinism and emergence, oviposition,and fecundity of the genera Ptychopteraand Paraleptophiebia. 69

18. Potential bases for detritivorenutrition. 75

19. Commonly used measuresof food quality. 76

20. Options of detritivoresfeeding on a nutritionally poor resource. 78 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 toa 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 dependon 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 microbesmay 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 Paraleptophiebiaspp.

(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 Consumption Morphology Behavior

Gut Tract / Morphology / Microbiology Biochemistry Growth Survival Assimilation (Reproduction)

Gut Content Passage Time

II, Feces Egestion

Figure 1. MATERIALS ANI) METHODS

Organisms

Larvae1 ofPtychoptera 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 thanwere 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 isused 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) and bigleaf maple (Acer inacrophyllum). 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 Temper-pparatus2 Repli- Estimated 4ean Initial iment (days) aure ation Dry 1ass (mg) (n) C) Ptychoptera Paralepto- townesi phiebia spp.

5 1 24 11 1 10-12:3 3.67±0.93(53) 0.26±0.09(51) 0.40*0.11(48) 0.74*0.20(46)

6 2 16 10 2 1:125.37±2.08(32) 17 15 1 8;4 0.49±0.22(129)

7 3 17 15 3. 8;4 0.49±0.22(129)

8 4 42 11 1 17:1 0.15*0.05(35)

9 5 54 15 1 15:40.08±0.02(53)

10 6 21 12 1 15:20.42*0.11(59) 0.58±0.14(59)

11 7 23 5 1 7;2 0.69±0.28(31)

12 14 10 2 1;8-26 0.75*0.19(37) 0.39±0.18(40)

13 1 4 2 1;5-17 4.49±0.23(17) 0.54*0.27(4) 10 2 1:22-264.22±0.27(22) 0.65*0.06(26)

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 simulatingthe field environment at the time the animals were collected, and temperature control via incubatoror cold room were maintained during all laboratory experiments.

2i aerated 500-mi. Ehrlenmeyer flasks; 2individually aerated vials; 3 f low-through chambers.

3Number of animalsper replicate; number of replicates per treatment. 4Mean initialdry 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

2BetterEquipment 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 whichgroups 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 determinedon 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 accordingto 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 losson wetting by a factor of 1.31% (± 1.13%; n=12). Similarly, sediments were corrected for experimentalerror owing to incomplete recovery from the vials by 1.92% (± 0.41%; n9) and for an additional sievingerror 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 responsiveto 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 themass 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 samplesat

50°C and ashing themat 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 theywere 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% ethylalcohol, and run through a dilution series. The dilution series for

all samples consisted of 70:30; 50:50; 30:70ethyl 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; Lautenschlageret al. 1978),

mounted on stubs, vacuum-coated witha 60:40

gold-palladium alloy, and examined witha 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 bya psteriori contrasts, Tukeys test (J.L. Gill,personal communication; Gill

1978). The modified test statistic used for experiments

with unbalanced replicationwas: ( 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 bya 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 channelare 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 ata

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 depositionalareas 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 andorganic content of particles less than 1nun in diameter (mean percentage ± standarddeviation) from Berry Creek (Benton County,Oregon) riffles and pools both upstream from an3. within the flow- controlled portion ofthe channel.

Substrate Particle size fraction location ri < 53 urn 53-125 urn 125-250urn 250-500urn 500urn-i tam

Percentage of FPQM (less than 1 mm) portion: Upstream from bypass: Riffle 1015.05(±3.04) 7.66(±l.55)8.80(l.l4) 20.79(1.45) 47.71(i4.81) Pool 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: Riffle10 22.63(*3.54) 24.91(±1.68) 15.31(±l.17) 15.l0(±l.45) 22.07(±3.60) Pool 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: Riffle10 ].3.60(±1.45) l0.73(*2.06)8.26(±0.95)8.12(±0.79)8.96(±0.70) Pool 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: Riffle10 15.40(*2.18) 19.59(±4.90) 15.83(±l.71) 21.79(*7.46) 15.26(2.56) Pool 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 9.4± 3.3 side channel 12.7± 2.2 embedded stones 10.4± 1.4 undercut bank 7.3± 3.9 Depositional under leaves 26.0± 17.2 log jam 29.1± 13.1 leaf pack 47.6± 12.0 channel 31.9± 10.6 moss 73.9± 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 mayflieswere 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 ina 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. The mayf lies are less active in the sediment. 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. Para1eptopilebia spp. Habitat Reference Habitat Reference

Decaying vegetation 1,3,4,5,7,10, Swift water, slowly8,10,13,14 in shallow water 11,15,16,18 to moderately flow- 17,22,P ing riffles

Organic sediment l,3,5,7,19,20,PLeaf debris l0,17,P

Springs. and slowly l0,P Tops and sides of 13, P flowing streams rocks

Bogs (PR 4-5.6) 4 Beneath rocks 9, l7,P

Tributary mouths 12,21, P (areas of high Fe concentration)

Bittacomorpha, a 23 Holarctic distribu- 6 related genus, has tion. In Nearctic, widespread distribution general throughout in North America North America

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 andBrusven 1970; 14. Rynes 1970; 15. Wirth and Stone 1971; 16. Hodkinson 1973; 17.Edmunds et a].. 1976; 18. Pennak 1978; 19. Wagner 1978; 20. Tolkamp1980; 21. Harris et a).. 1981; 22. Pereira 1981; 23. Merritt and Cummins 1984;P. Present study. 27 particles occur (Table 4). Lehm]cuhl and Anderson (1971), however, note that 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 Paraleptophiebiaspp. differ in their requirements and ability to colonize stream habitats.

This is supported by studies with artificialstream 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 poolareas (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 sameas 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 habitatas 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. Comparative survival and growth (mean ± standard error) of Ptychoptera townesi and Paralepto- phiebia spp. on coarse and fine particulate organic matter (Experiment 1).

Substrate Substrate Ptychoptera townesi Paraleptophlebia spp. organic content Survival Relative growthSurvival Relative growth (%) (%) rate(% body wt/d) (%) rate (% body wt/d)

UPOM 21.9 90 0.35 0.20 47 033 ± 0.23 (0.45-53 urn)

FPOM 27.2 100 -0.44 ± 0.26 53 0.57 ± 0.30 (53-250 urn)

Alder leaves 85.4 87 -0.82 ± 0.19 79 3.31 ± 0.24 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 Paralepto- phiebia spp.(± standard error) on FPOM size fractions of ground, leached alder particles (Experiment 2).

Ptychoptera townesi Paraleptophlebia spp.

Alder particleSurviva1 Relative growth Survival Relative growth size range (urn) (%) rate (% body wt/d) (%) 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

500-1 nun --- Ni) 75 -0.53*0.66

* 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 Substrate Animal Relative particle size organic content survival growth rate range (%) (%) (% 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

1-4 mm 84.6 75 0.81 ± 0.81 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 drymasses (± standard error) of early instar Paralepto- phiebia spp. on particle size fractions of Berry Creek sediment (Experiment 4).

Substrate Substrate Animal 1ean final Relative growth particle organic survival dry wt (mg) rate (% body wt/d) size content (%) range (%)

< 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. 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).

Site Substrate Survival Relative growth rate organic content (%) (% body wt/day) (%)

Muskeg Creek 24.1 78 2.80 0.28

UpperLeft 5.4 53 2.20 0.20 Fork

UpperControl18.2 63 2.05± 0.21 Creek

LowerRight 7.6 35 1.87* 0.35 Fork

LowerBeach 13.9 30 1.41± 0.52 Creek

LowerTrap 5.4 ii. 0.83± 0.69 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 Substrate Survival Relative growth rate particle size organic (%) (% body wt/d) range (urn) content (%)

Elk Creek 53-125 0.40 93 1.15 0.09 l25 250 0.26 57 0.38 0.26 (least affected

Upper Clearwater53-125 0.23 3 0.74 125-250 0.25 0

Middle 53-3.25 1.03 83 0.64 j 0.13 Clearwater 125-250 1.61 10 -0.68

Muddy River 53-125 0.18 3 -2.09 125-250 0.17 0

Ape Canyon 53-125 0.16 0 125-250 0.18 0 (most affected

* Personal observation; K.W. Cummins, personalcommunication. 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 Substrate Survival Relative growth rate particle size organic (% body wt/d) range (urn) content (%)

Yellowjacket 53-125 3.4 Creek 0 *125-250 1.5 100 (least affected -1.47 ± 0.26 Elk Creek 53-125 1.6 0 125-250 1.1 67 -1.27 t 0.34 Middle Clearwater 53-125 0.7 33 -0.47 125- 250 0.7 100 -0.64 ± 0.43 Lake Creek 53-125 7.3 67 -1.19 ± 0.29 * 125-250 2.9 100 (most affected -2.44 * 0.69

* C.p. Hawkins, persona]. communication. 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

Figure 2. 43

Figure 3. Photographs (a) of red alder leaf disks fedon 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

H4i:

e f

Figure 3. 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), withan 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

Figure 4. 48 capacious of the three gut regions, in many cases larger than the hindgut by a factor of ten. This is true as well for Paraleptophiebia spp. 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 0.1mm in length was frequently observed around the anterior portion of the hindgut of Ptychoptera townesi, the gut tracts of this species and Paraleptophiebiaspp. are not discolored in the same way as are those of invertebrates withgut regions of high pH. Further investigations using a pH microelectrode showed that none of these animals hasa 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 feedon 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 10-25°c (Zimmerman and

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 Paraleptophiebiaspp. are variable. Determinations with dyed cellulose mixed with

Berry Creek sediment (less than 500 urn, at 10°c) yielded values greater than 19ri for Ptychoptera townesi and less than 3 h for Paraleptophlebiaspp. 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 fora 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 Paraleptophlebiaspp. 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 falsecrane 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). Yet, assimilation is known to be variable. 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). No animals maintained at 18°C survived. 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 Ptychop- t8ra townei and paraleptophiebia spp. at 4 C and 10 C.

Temperature Ptychoptera townesi Paraleptophiebia spp. (°C) Egestion rate Egestion rate Daily Relative ily Relative n (mg/d) (xng/mg/d) n (mg/d) (ing/mg/d)

40 17 0.15 ± .02 0.03 ± .01 5 0.04 ± .01 0.07 ± .02

100 C 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

0 0 20 30 40 50 60

-C

E C

-E

0 10 20 30 40

0 0 OO4 I (c)

0.03- \i .c C o ' O.O2- E 'WV"

['I'll

0 10 20 30 40 5 20 40 60 80 130 I Figure 5. TIME (h) 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 0.042mg 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 Paraleptophlebia app.

Substrate Substrate Survival Relative Survival Relative organic (%) growth rate (%) growth rate content (% body wt/d) (% body wt/d) (%)

Alder leaves 87.9 90 -1.03 ± 0.05 46 2.08 ± 1.23 Ptychoptera townesi feces 50.0 85 -1.27 ± 0.06 ND OPOM + alder leaves 46.5 80 -0.05 ± 0.27 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).

* Ptychoptera townesi Paraleptophlebia spp. Substrate Survival Relative growth Survival Relative growth (%) rate (% body wt/d) (%) 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

Feces (53-500 urn) from shredders fed alder leaves 75 0.36 ± 0.11 31 0.48

* Organic content, 78-79%. 67

Table 16. 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).

Ptychoptera townesi Paraleptophlebia spp. * Substrate Survival Relative growthSurvival Relative growth (%) rate (% body wt/d) (%) rate (% body wt/d)

Alder leaves 50 -0.90 ± 0.56 67 1.88 * 0.92

Feces (250-500 urn) from shredders fed alder leaves 100 -0.84 ± 0.30 50 0.63 ± 0.53

* 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

1971). The life cycle of Paraleptophiebia gregalis is 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. Ptychoptera townesi 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. Paraleptophlebia spp. Reference Reference

Voltiriisxa and Emergence: Uru.voltine Univoltine -extended, May-July 9 -spring and fall 7,8,11, -spring arid summer 1,7,? 1.2,13,?

Bivoltine 2

MultivOltine 5 "expanded' 13 Adults emerge pupae move from water to 1 from water surface moist ground 6,11 Adults emerge from water 15,? surface Oviposition:

In sphagnum at water surface3 At water surface 11 Fecundity:

Average number of eggs 2 Average number of eggs 4,10 laid, 554 in subimagoes, 264-1160

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 andBoerger 197411. Edmurids et al. 1976; 12. Sliapas and Hilserthoff 1976; 13. Corkum 1978;1.4. arTs and Carlson 1978; 15. Andersonand 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%. This is higher than larvae of Ptychoptera townesi, 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. in addition, they are quite mobile. 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. It is probably too large for reirigestion. 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. Potential bases for detritivore nutrition.

Basis Reasoning References

PARTICLE SUBSTRATE: Sheer quantity Cammen et al. 1978; Levjnton 1979

Not enough microbes Baker and Bradnam 1976; Cammen et in number, biomass, or al. 1978; Tunnicliffe and Risk 1977; nutrient content flndlay et al. 1984

Easily digested portions Lopez et al. 1977

Nitrogen-rich portions TenOre 1977; LevintOrt and Bianchi 1981

Benthic diatoms may be Johannes and Satomi 1966; Fenchel locally important 1969 ATTACHED, ASSOCIATED, AND INTERSTITUAL MICROBES: Live on bacteria alone Fredeen 1964

Only microbes are Hargrave 1970; Marchant and Hynes digested 1981

Use bacterial epigrowth Newell 1965; Fenchel 1970; Lopez and Levinton 1978; Rounic}c and Winterbourn 1983 Bacteria are major source Newell 1965, 1970; Hargrave 1970; FenChel 1970

Use microbes attached to Smyly and Collins 1975 algae

Use epilithic detritus Madsen 1972; Calow 1975c through bacteria

Microbes provide more Baker and Bradnam 1976; complete nitrogen or Bàrlocher and Kendrick 1973 growth factors

Directly or indirectly Newell 1965; Fenchel 1970; Wavre (substrate alteration) 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 Adams and Angelovic 1970; Stephens Arthropoda and Schineke 1961; Sepers 1977; Stephens 1982 Ingest colloids and Wotton 1976, 1982 surface film

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.

Options References

* Alteration of ingestion rate Cummins and Kiug 1979; Taghon 1981 * Alteration of gut passage time Calow 1975b, 1977

Alteration of digestive Fredeen 1964; Chua and Brinkhurst capability or absorption rate 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 Cummins and Klug 1979 of ingested food to body

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 Wieser 1956; Becker 1958; Cummins separation 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 thedeposit-feeder guild, because these organisms are "bulkfeeders" (i.e., they feed on masses of particles rather thn ingesting them individually).

Fauchald and Jumars(1979) distinguish between

"macrophages," thathandle food items singly and

"microphages," thathandle 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). System alterations undeniably affect organisms. 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

LITERATURE CITED

Adams, S.M. and J.W. Angelovic. 1970. Assimilation of detritus and its associated bacteria by three species of estuarine animals. Chesapeake Science 11:249-254.

Alexander, C.P. 1920. The crane-flies of New York. Part II. Biology and phylogeny. Cornell University Agricultural Experiment Station Memoir 38:691-1133.

Anderson, J.M. and A. Macfadyen, Eds. 1976. The role of terrestrial and aquatic organisms in decomposition processes. Blackwell Scientific Publications. Oxford. 474 pp.

Anderson, N.H. 1976. Carnivory by an aquatic detritivore, Clistoronia magnifica (Trichoptera: Limnephilidae). Ecology 57:1081-1085.

Anderson, N.H. and K.W. Cununins. 1979. Influences of diet on the life histories of aquatic insects. Journal of the Fisheries Research Board of Canada 36:335-342.

Anderson, N.H. and E. Grafius. 1975. Utilization and processing of allochthonous material by stream Trichoptera. Verhandlungen der Internationalen Vereinigung für theoretische und angewandte Limnologie 19:3083-3088.

Anderson, N.H. and J.B. Wallace. 1984. Habitat, life history, and behavioral adaptations of aquatic insects, pp. 38-58. In: R.W. Merritt and K.W. Cummins, eds. An introduction to the aquatic insects of North America (second edition). Kendall/Hunt. Dubuque.

Appleby, A.G. and R.0. Brinkhurst. 1970. Defecation rate of three tubificid oligochaetes found in the sediment of Toronto Harbour, Ontario. Journal of the Fisheries Research Board of Canada 27:1971-1982.

Baker, J.H. and L.A. Bradnam. 1976. The role of bacteria in the nutrition of aquatic detritivores. Oecologia (Berlin) 24:95-104.

Bärlocher, F. 1982. The contribution of fungal enzymes to the digestion of leaves by Gammarus fossarum Koch (Amphipoda). Oecologia (Berlin) 52:1-4.

Bärlocher, F. and B. Kendricic. 1973. Fungi and food preferences of Gammarus pseudolimnaeus. Archiv für Hydrobiologie 72:501-516.

Bärlocher, F. and B. Kendrick. 1975. Assimilation efficiency of Gammarus pseudolimnaeus (Axnphipoda) feeding on fungal mycelium or autumn-shed leaves. Oilcos 26:55-59.

Becker, p. 1958. The behavior of larvae of Culicoides circumscriptus Kieff. (Dipt., Ceratopogonidae) towards light stimuli as influenced by feeding, with observations on the feeding habits. Bulletin of Entomological Research 49: 785-802.

Berenbaum, M. 1980. Adaptive significance of midgut pH in larval Lepidoptera. The American Naturalist 115:138-146.

Bernays, E.A. and S.J. Simpson. 1982. Control of food intake. Advances in Insect Physiology 16:59-118.

Berrie, A.D. 1976. Detritus, microorganisms and animals in freshwater, pp. 323-338. In: J.M.. Anderson and A. MacFadyen, eds. The role of terrestrial and aquatic organisms in decomposition processes. Blackwell Scientific Publications. Oxford.

Bjarnov, N. 1972. Carbohydrases in Chironomus, Gammarus and some Trichoptera larvae. Oikos 23:261-263.

Bolton, P.J. and J. Phillipson. 1976. Burrowing, feeding, egestion and energy budgets of Allolobophora rosea (Savigny)(Lumbricidae). oecologia (Berlin) 23: 225-245.

Bowen, S.H. 1979. A nutritional constraint in detritivory by fishes: the stunted population of Sarotherodon mossambicus in Lake Sibaya, South Africa. Ecological Monographs 49:17-31.

Brennan, A., A.J. McLachlan, and R.S. Wotton. 1978. Particulate material and nudge larvae (Chironomidae: Diptera) in an upland river. Hydrobiologia 59:67-73.

Brinkhurst, R.0., K.E. Chua, and N.K. Kaushik. 1972. Interspecific interactions and selective feeding by tubificid oligochaetes. Limnology and Oceanography 17:122-133.

Brittain, J.E. 1982. Biology of mayflies. Annual Review of Entomology 27:119-147.

Buchner, P. 1965. Endosymbiosis of animals with plant microorganisms (revised. English version). Interscience Publishers. New York. 909 PP.

Buikema, A.L., Jr. and E.F. Benfield. 1979. Use of macroinvertebrate life history information.in toxicity tests. Journal of the Fisheries Research Board of Canada 36: 321-328.

Buikema, A.L., Jr., J.G. Geiger, and D.R. Lee. 1980. Daphnia toxicity tests, PP. 48-69. In: A.L. Buikema, Jr. and J. Cairns, Jr., eds. Aquatic invertebrate bioassays. ASTM STP 715. American Society for Testing and Materials.

Calow, P. 1975a. The feeding strategies of two freshwater gastropods, Ancylus fluviatilis Mull, and Planorbis contortus Linn. (Pulmonata), in terms of ingestion rates and absorption efficiencies. Oecologia (Berlin) 20:33-49.

Calow, P. 1975b. Defaecation strategies of two freshwater gastropods, Ancylus fluviatilis Mull and Planorbis contortus Linn. (Pulmonata) with a comparison of field and laboratory estimates of food absorption rate. Oecologia (Berlin) 20:51-63.

Calow, P. 1975c. On the nature and possible utility of epilithic detritus. Hydrobiologia 46:181-189.

Calow, P. 1977. Ecology, evolution and energetics: a study in metabolic adaptation.Advances in Ecological Research 10:1-62.

Cammen, L.M. 1980. The significance of microbial carbon in the nutrition of the deposit feeding polychaete Nereis succinea. Marine Biology 61:9-20.

Cammen, L., P. Rublee, and J. Hobbie. 1978. The significance of microbial carbon in the nutrition of the polychaete Nereis succinea and other aquatic deposit feeders. UNC Sea Grant Publication UNC-SG-78-12.

Carefoot, T.H. 1973. Feeding, food preference, and the uptake of food energy by the supralittoral isopod Ligia pallasii. Marine Biology 18:228-236.

Chance, M.M. 1970. The functional morphology of the mouthparts of blackfly larvae (Diptera: Simuliidae). Quaestiones Entomologicae 6: 245-284.

Chapman, D.W. and R. Demory. 1963. Seasonal changes in the food ingested by aquatic insect larvae and nymphs in two Oregon streams. Ecology 44:140-146. Chua, ICE. and R.O. Brinkhurst. 1973. Evidence of interspecific interactions in the respiration of tubificid oligochaetes. Journal of the Fisheries Research Board of Canada 30:617-622.

Clifford, H.F. and H. Boerger. 1974. Fecundity of mayflies (Ephemeroptera), with special reference to mayflies of a brownwater stream of Alberta, Canada. Canadian Entomologist 106:1111-1119.

Clifford, H.F., H. Hamilton, and B.A. Killins. 1979. Biology of the mayfly Leptophlebia cupida (Say) (Ephemeroptera: Leptophlebiidael. Canadian Journal of Zoology 57:1026-1045.

Cook, R.J., J.C. Barron, R.I. Papendick, and G.J. Williams III. 1980. Impact on agriculture of the Mount St. Helens eruptions. Science 211:16-22.

Corkum, L.D. 1978. The nymphal development of Paraleptophlebia adoptiva (McDunnough) and Paraleptophiebia mollis (Eaton) (Ephemeroptera: Leptophlebiidae) and the possible influence of temperature. Canadian Journal of Zoology 56:1842-1846.

Cummins, K.W. 1964. Factors limiting the microdistribution of larvae of the caddisflies, Pycnopsyche lepida (Hagen) and Pycnopsyche guttifer (Walker) in a Michigan stream (Trichoptera: Limnephilidae). Ecological Monographs 34:271-295.

Cummins, K.W. 1973. Trophic relations of aquatic insects. Annual Review of Entomology 18:183-206.

Cummins, K.W. 1974. Structure and function of stream ecosystems. BioScience 24:631-641.

Curnmins, K.W. 1975. Macroinvertebrates, pp. 170-198. In: B.A. Whitton, ed. River ecology. Studies in Ecology. Volume 2. University of California Press. Berkeley.

Cummins, K.W. and M.J. Kiug. 1979. Feeding ecology of stream invertebrates. Annual Review of Ecology and Systematics 10:147-172.

Cummins, K.W. and G.L. Spengler. 1978. Stream ecosystems. Water Spectrum 10:1-9.

Cummins, K.W., M.J. Kiug, G.M. Ward, G.L. Spengler, R.W. Speaker, RW. Ovink, D.C. Mahan, and R.C. Petersen. 1981. Trends in particulate organic matter fluxes, community processes and macroinvertebrate functional groups along a Great Lakes Drainage Basin river continuum.Verhandlungen der Internationalen Vereinigung für theoretische und angewandte Limnologie 21:841-849.

Cuinmins, K.W., R.C. Petersen, F.0. Howard, J.C. Wuycheck, and V.1. Holt. 1973. The utilization of leaf litter by stream detritivores. Ecology 54:336-345.

Davies, I.J. 1975. Selective feeding in some arctic Chironomidae. Verhandlungen der Internationalen Vereinigung für theoretische und angewandte Limnologie 19: 3149-3154.

Dermott, R. 1981. Ingestion rate of1he burrowing mayfly Hexagenia limbata as determined with C. Hydrobiologia 83 :499-503.

Dickinson, C.H. and G.J.F. Pugh. Eds. 1974. Biology of plant litter decomposition. Academic Press. New York. Vol. I, 146 pp. Vol. II, 175 pp.

Edinunds, G.F., Jr., S.L. Jensen, and L. Berner. 1976. The mayf lies of North and Central America. University of Minnesota Press. Minneapolis. 330 pp. Egglishaw, H.J. 1964. The distributional relationship between the bottom fauna and plant detritus in streams. Journal of Animal Ecology 33:463-476.

Eriksen, C.H. 1964. The influence of respiration and substrate upon the distribution of burrowing mayfly naiads. Verhandlungen der Internationalen vereinigung für theoretische und angewandte Limnologie 15:903-911.

Fauchald, K. and P.A. Jumars. 1979. The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology, An Annual Review 17:193-284.

Fenchel, T. 1969. The ecology of marine microbenthos. IV. Structure and function of the benthic ecosystem, its chemcial and physical factors and the microfauna communities with special reference to the ciliated Protozoa. Ophelia 6:1-182.

Fenchel, T. 1970. Studies on the decomposition of organic detritus derived from the turtle grass, Thalassia testudinum. Limnology and oceanography 15:14-20.

Fenchel, T., L.H. Kofoed, and A. Lappalainen. 1975. Particle size-selection of two deposit feeders: the amphipod Corophium volutator and the prosobranch Hydrobia ulvae. Marine Biology 30:119-128. Findlay, S., J.L. Meyer, and P.J. Smith. 1984. Significance of bacterial biomass in the nutrition of a freshwater isopod (Lirceus sp.). oecologia (Berlin) 63:38-42.

Fredeen, F.J.H. 1964. Bacteria as food for blackfly larvae (Diptera: Simuliidae) in laboratory cultures and in natural streams. Canadian Journal of Zoology 42:527-548.

Fruchter, J.S., D.E. Robertson, J.C. Evans, K.B. Olson, E.A. Lepel, J.C. Laul, K.H. Abel, R.W. Sanders, P.O. Jackson, N.S. Wogman, R.W. Perkins, H.H. van Tuyl, R.H. Beauchamp, J.W. Shade, J.L. Daniel, R.L. Erikson, G.A. Sehmel, R.N. Lee, A.V. Robinson, O.R. Moss, J.K. Briant, and W.C. Cannon. 1980. Mount St. Helens ash from the 18 May 1980 eruption: chemical, physical, mineralogical, and biological properties. Science 209:1116-1125.

Geesey, G.G., R. Mutch, J.W. Costerton, and R.J. Green. 1978. Sessile bacteria: an important component of the microbial population in small mountain streams. Limnology and Oceanography 23:1214-1223.

Gersich, F.M. and M.A. Brusven. 1982. Volcanic ash accumulation and ash-voiding mechanisms of aquatic insects. Journal of the Kansas Entomological Society 55:290-296.

Gill, J.L. 1978. Design and analysis of experiments in the animal and medical sciences. The Iowa State University Press. Ames, Iowa. Vol. I, 409 pp. Vol. III, 173 pp.

Gilpin, B.R. and M.A. Brusven. 1970. Food habits and ecology of mayflies of the St. Manes River in Idaho. Melanderia 4:19-40.

Gilson, W.E. 1963. Differential respirometer of simplified and improved design. Science 141:531-532.

Gray, J.S. 1966. The attractive factor of intertidal sands to Protodrilus symbioticus. Journal of the Marine Biology Association of the United Kingdom 46:627-646.

Gray, L. 1979. The use of psychophysical unfolding theory to determine principal resource axes. The American Naturalist 114:695-706.

Gurtz, M.E., J.R. Webster, and J.B. Wallace. 1980. Seston dynamics in southern Appalachian streams: effects of clear-cutting. Canadian Journal of Fisheries and 91

Aquatic Sciences 37:624-631.

Hanson, B.J. 1983. Lipid content and fatty acid composition of aquatic insects: dietary influence and aquatic adaptation. Ph.D. Thesis. Oregon State University, Corvallis. 143 pp.

Hanson, R.B. and W.J. Wiebe. 1977. Heterotrophic activity associated with particulate size fraction in a Spartina alterniflora salt-marsh estuary, Sapelo Island, Georgia, USA, and the continental shelf waters. Marine Biology 42:321-330.

Hargrave, B.T. 1970. The effect of a deposit-feeding amphipod on the metabolism of benthic microflora. Limnology and Oceanography 15:21-30.

Hargrave, B.T. 1972. Prediction of egestion by the deposit-feeding amphipod Hyalella azteca. Oikos 23:116-124.

Harper, R.M., J.C. Fry, and M.A. Learner. 1981. A bacteriological investigation to elucidate the feeding biology of Nais variabilis (Oligochaeta: Naididae). Freshwater Biology 11:227-236.

Harris, S.C. and R.B. Carlson. 1978. Distribution of Bittacoinorpha clavipes (Fabricius) and Ptychoptera quadrifasciata Say (Diptera: Ptychopteridae) in a sandhill springbrook of southeastern North Dakota. Annual Proceedings of the North Dakota Academy of Science 29:59-66.

Harris, S.C., R.B. Carlson, and E.U. Balsbaugh, Jr. 1981. Ecological distribution of insects in two streams of the sandhills of southeastern North Dakota. North Dakota Insects -- Schafer - Post Series No. 13. North Dakota State University. Fargo. 112 pp.

Hodkinson, I.D. 1973. The immature stages of Ptychoptera lenis lenis (Diptera: Ptychopteridae) with notes on their biology. Canadian Entomologist 105:1091-1099.

Hooper, P.R., I.W. Herrick, E.R. Laskowski, and C.R. Knowles. 1980. Composition of the Mount St. Helens ashfall in the Moscow-Pullman area on 18 May 1980. Science 209:1125-1126.

Howard, F.0. 1975. Natural history and ecology of Pycnopsyche lepida, P. guttifer and P. scabripennis (Trichoptera: Limnephilidae) in a wo3dland stream. Ph.D. Thesis. Michigan State University. East Lansing. 115 pp. Howarth, C.J. 1977. The Carlo Erba analyzer; carbon, hydrogen, nitrogen, and oxygen, pp. 75-117. In: R.Belcher, ed. International organic elemental analysis. Academic Press.

Hylleberg, J. and V.F. Gallucci. 1975. selectivity in feeding by the deposit-feeding bivalve Macoma nasuta. Marine Biology 32:167-178.

Hylleberg Kristensen, J. 1972. Carbohydrases of some marine invertebrates with notes on their food and on the natural occurrence of the carbohydrates studied. Marine Biology 14:130-142.

Hynes, H.B.N. 1970. The ecology of running waters. University of Toronto Press. 555 pp.

Ide, F.P. 1940. Quantitative determination of the insect fauna of rapid water. University of Toronto Stud. Fish. Res. Lab. 59:1-20.

Iversen, T.M. 1974. Ingestion and growth in Sericostoma personatum (Trichoptera) in relation to the nitrogen content o ingested leaves. Oikos 25:278-282.

Iversen, T.M. and B.L. Madsen. 1978. Allochthonous organic matter in streams. Folia Limnologica Scandinavica 17-20.

Jaksi, F.M. 1981. Abuse and misuse of the term °guild" in ecological studies. Oikos 37:397-400.

Johannes, R.E. and M. Satomi. 1966. CompositiOn and nutritive value of fecal pellets of a marine crustacean. Limnology and Oceanography 11:191-197.

Johannes, R.E., S.J. Coward, and K.L. Webb. 1969. Are dissolved amino acids an energy source for marine invertebrates? Comparative Biochemistry and Physiology 29:283-288.

Johannsen, O.A. 1934. Aquatic diptera. Part I. Neinocera, exclusive of Chironomidae and Ceratopogonidae. Cornell University Agriculture Experiment Station Memoir 164. 95 pp.

Jonasson, P.M. 1972. Ecology and production of the profundal benthos in relation to phytoplankton in Lake Esrom. Oikos Suppi. 14:1-148. 93

Kaushik, N.K. and H.B.N. Hynes. 1971. The fate of the dead leaves that fall into streams. Archiv für Hydrobiologie 68:465-515.

King, R.H. 1978. Natural history and ecology of Stictochironoinus annulicrus (Townes) (Diptera: Chironomidae), Augusta Creek, Kalamazoo County, Michigan. Ph.D. Thesis. Michigan State University, East Lansing. 156 pp.

Kirby-Smith, W.W. 1976. The detritus problem arid the feeding and digestion of an estuarine organism, pp. 469-480. In: M. Wiley, ed. Estuarine Processes. Vol. 1. Uses, stresses, and adaptation to the estuary.Academic Press. New York.

Klots, E.B. 1966. The new field guide of freshwater life. G.P. Putnam and Sons. New York. 398 pp.

Klug, M.J. and S. Kotarski. 1980. Bacteria associated with the gut tract of larval stages of the aquatic cranefly Tipula abdominalis (Diptera: Tipulidae).Applied and Environmental Microbiology 40:408-416.

Kraft, G.F. 1964. Seasonal occurrence and distribution of aquatic insects in Berry Creek. Ph.D. Thesis. Oregon State University. Corvallis. 122 pp. Krogh, A. 1939. Osmotic regulation in aquatic animals. Cambridge University Press. London. 242 pp.

Ladle, M., J.A.B. Bass, and W.R. Jenkins. 1972. Studies on production and food consumption by the larval Simuliidae (Diptera) of a chalk stream. Hydrobiologia 39:429-448.

Laughlin, R. 1967. Biology of Tipula paludosa; growth of the larva in the field. Entomologia experimentalis et applicata 10: 52-68.

Lautenschlager, K.P., N.K. Kaushik, and J.B. Robinson. 1978. The peritrophic membrane and faecal pellets of Gammarus lacustris limnaeus Smith. Freshwater Biology 8:207-211.

Lehmkuhl, D.M. 1969. Biology and downstream drift of some Oregon Ephemeroptera. Ph.D. Thesis. Oregon State University. Corvallis. 110 pp.

Lehmkuhl, D.M. 1979. Environmental disturbance and life histories: principles and examples. Journal of the Fisheries Research Board of Canada 36:329-334. 94

Lehmkuhl, D.M. and N.H. Anderson. 1971. Contributions to the biology and taxonomy of the Paraleptophiebia of Oregon (Ephemeroptera: Leptophlebiidae). The Pan-Pacific Entomologist 47 :85-93.

Leonard, J.W. and F.A. Leonard. 1962. Mayf lies of Michigan trout streams. Bulletin No. 43. Cranbrook Institute of Science. Bloomfield Hills, Michigan. 139 pp.

Levinton, J. 1972. Stability and trophic structure in deposit-feeding and suspension-feeding communities. The American Naturalist 106:472-486.

Levinton, J.S. 1979. Deposit-feeders, their resources, and the study of resource limitation,pp. 117-141. In: R.J. Livingston, ed. Ecological processes in coastal and marine systems. Plenum Press. New York. 548 pp.

Levinton, J.S. and T.S. Bianchi. 1981. Nutrition and food limitation of deposit-feeders. I. The role of microbes in the growth of mud snails (Hydrobiidae). Journal of Marine Research 39:531-545.

Lopez, G.R. and J.S. Levinton. 1978. The availability of microorganisms attached to sediment particles as food for Hydrobia ventrosa Montagu (Gastropoda: Prosobranchia). Oecologia (Berlin) 32:263-275.

Lopez, G.R., J.S. Levinton, and L.B. Slobodkin. 1977. The effect of grazing by the detritivore Orchestia grillis on Spartina litter and its associated microbial community. Oecologia (Berlin) 30:111-127.

Lowry, I.E., N.J. Rosebrough, A.L. Farr, and R.J. Randall. 1951. Protein measurements with folin phenol reagent. Journal of Biological Chemistry 193:265-275.

Mackay, R.J. 1969. Aquatic insect communities of a small stream on Mont St. Hilaire, Quebec. Journal of the Fisheries Research Board of Canada 26:1157-1183.

Mackay, R.J. and J. Kalff. 1973. Ecology of two related species of caddis fly larvae in the organic substrates of a woodland stream. Ecology 54:499-511.

MacMahon, J.A., D.J. Schimpf, D.C. Andersen, K.G. Smith, and R.L. Bayn, Jr. 1981. An organism-centered approach to some community and ecosystem concepts. Journal of Theoretical Biology 88:287-307. Madsen, B.L.1972.Detritus on stones in small streams. Memorie deli' Istituto di Idrobiologia 29 Suppl.:385-403. Mahmud-ulAmeen.1969.Metamorphosis of some of the organ systems in the fly Ptychoptera aibimana F.Transactions of the Royal Entomological Society of London 121:235-279. Malmqvist, B., L.M. Nilsson, and B.S. Svensson.1978. Dynamics of detritus in a small stream in southern Sweden and its influence on the distribution of the bottom animal communities.Oikos 31:3-16. Marchant, R. and H.B.L'T. Hynes.1981.Field estimates of feeding rate for Gammarus pseudolimnaeus (Crustacea: Amphipoda) in the Credit River, Ontario.Freshwater Biology 11:27-36. Martin, M.M., J.S. Martin, J.J. Kukor, and R.W. Merritt. 1980.The digestion of protein and carbohydrate by the stream detritivore, Tipula abdominalis (Diptera, Tipulidae).Oecologia (Berlin) 46:360-364. Mattingly, R.L.Mass loss and qualitative change in stream-incubated fine particulate organic matter derived from leaves differing in rate of processing.Submitted to Hydrobiologia. Mattingly, R.L., K.W. Cummins, and R.H. King.1981. The influence of substrate organic content on the growth of a stream chironomid.Hydrobiologia 77:161-165. Mattson, W.J., Jr.1980.Herbivory in relation to plant nitrogen content.Annual Review of Ecology and Systematics 11:119-161. Mccullough, D.A., G.W. Minshali, and C.E. Cushing.1979. Bioenergetics of a stream "collector" organism, Tricorythodes minutus (Insecta: Ephemeroptera).Limnology and Oceanography 24:45-58. McLachlan, A.J.1977.Some effects of tube shape on the feeding of Chirononius plumosus L. (Diptera: Chirononiidae). Journal of Animal Ecology 46:139-146. McLachlan, A.J., A. Brennan, and R.S. Wotton.1978. Particle size and chironoinid (Diptera) food in an upland river.Oikos 31:247-252. McMahon, R.F., R.D. Hunter, and W.D. Russell-Hunter. 1974.Variation in aufwuchs at six freshwater habitats in terms of carbon biomass and of carbon:nitrogen ratio. Hydrobiologia 45:391-404. Meadows, P.S. 1964a. Experiments on substrate selection by Corophium species: films and bacteria on sand particles. Journal of Experimental Biology 41:499-511.

Meadows, P.S. 1964b. Substrate selection by Corophium species: the particle size of substrates. Journal of Animal Ecology 33:387-394.

Meadows, P.S. 1965. Attachment of marine and fresh-water bacteria to solid surfaces. Nature 207:1108.

Meitz, A.K. 1975. Alimentary tract microbiota of aquatic invertebrates. M.S. Thesis. Michigan State University. East Lansing. 64 pp.

Merritt, R.W. and K.W. Cuminins. (Eds.) 1984. An introduction to the aquatic insects of North America (second edition). Kendall/Hunt. Dubuque. 722 pp.

Miall, L.C. 1895. The natural history of aquatic insects. Macmillan and Co. New York. 395 pp.

Molongoski, J.J. and M.J. Kiug. 1976. Characterization of anaerobic heterotrophic bacteria isolated from freshwater lake sediments. Applied and Environmental Microbiology 31 :83-90.

Monk, D.C. 1976. The distribution of cellulase in freshwater invertebrates of different feeding habits. Freshwater Biology 6:471-475.

Moring, J.R. 1975. The Alsea watershed study: effects of logging on the aquatic resources of three headwater streams of the Alsea River, Oregon. Part II - Changes in environmental conditions. Fish. Res. Rept. No. 9. Res. Sect. Oregon Dept. Fish Wildi.

Mulla, M.S. and L.A. Lacey. 1976. Feeding rates of Siznulium larvae on particulates in natural streams (Diptera: Simuliidae). Environmental Entomology 5: 283-287.

Needham, J.G., J.R. Traver, and Y.-C. Hsu. 1935. The biology of mayf lies. Comstock Publishing Company, Inc. Ithaca, New York. 759 pp.

Newell, R. 1965. The role of detritus in the nutrition of two marine deposit feeders, the prosobranch Hydrobia ulvae and the bivalve Macoma balthica. Proceedings of the Zoological Society of London 144:25-45. 97

Newell, R.C. 1970. Biology of intertidal animals. Logos Press Limited. London. 555 pp.

Otto, C. 1974. Growth and energetics in a larval population of Potamophylax cingulatus (Steph.)(Trichoptera) in a South Swedish stream. Journal of Animal Ecology 43:339-361.

Paerl, H.W. and C.R. Goldman. 1972. Stimulation of heterotrophic and autotrophic activities of a planktonic microbial community by siltation at Lake Tahoe, California. Memorie dell' Istituto di Idrobiologia 29 Suppl. : 129-147.

Paerl, H.W. and S.L. Shimp. 1973. Preparation of filtered plankton and detritus for study with scanning electron microscopy. Limnology and Oceanography 18:802-805.

Pennak, R.W. 1978. Freshwater invertebrates of the United States (second edition). John Wiley and Sons. New York. 803 pp.

Pereira, C.R.D. 1981. Life history studies of Cinygnia integrum Eaton (Ephemeroptera: Heptageniidae) and other mayflies associated with wood substrates in Oregon streams. M.S. Thesis. Oregon State University. Corvallis. 92 pp.

Perkins, M.A. and L.A. Kaplan. 1978. Epilithic periphyton and detritus studies in a subalpine stream. Hydrobiologia 57 : 103-109.

Petersen, R.C. and K.W. Cummins. 1974. Leaf processing in a woodland stream. Freshwater Biology 4:343-368.

Peterson, A. 1960. Larvae of insects. An introduction to Nearctic species. Part II. Coleoptera, Diptera, Neuroptera, Siphonaptera, Mecaptera, Trichoptera (fourth edition). Edwards Bros., Inc. Ann Arbor. 416 pp.

Pomeroy, L.R. 1980. Detritus and its role as a food source, pp. 84-118. In: R.K. Barnes and K.H. Mann, eds. Fundamentals of aquatic ecosystems. Blackwell Scientific Publications. Oxford.

Porter, K.G. and Y.S. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25:943-948.

Prins, H.T. 1982. Why are mosses eaten in cold environments only? Oikos 38:374-380. Pritchard, G. 1978. Study of dynamics of populations of aquatic insects: the problem of variability in life history exemplified by Tipula sacra Alexander (Diptera; Tipulidae). Verhandlungen der Internationalen Vereinigung für theoretische und angewandte Limnologie 20:2634-2640.

Rabeni, C.F. and G.W. Minshall. 1977. Factors affecting microdistribution of stream benthic insects. Oikos 29: 33-43.

Rees, C.P. 1975. Competitive interactions and substratum preferences of two intertidal isopods. Marine Biology 30:21-25.

Rice, D.L. 1982. The detritus nitrogen problem: new observations and perspectives from organic geochemistry. Marine Ecology Program Series 9:153-162.

Richards, 0.W. and R.G. Davies. 1977. Imms general textbook of entomology. 10th edition. Volume 2: Classification and biology. Chapman and Hall. London. 1354 pp.

Ringler, N.H. and J.D. Hall. 1975. Effects of logging on water temperature and dissolved oxygen in spawning beds. Transactions of the American Fisheries Society 104: 111-121.

Rogers, J.S. 1933. The ecological distribution of the crane-flies of northern Florida. Ecological Monographs 3:1-74.

Rogers, J.S. 1942. The crane flies (Tipulidae) of the George Reserve, Michigan. Miscellaneous Publications, Museum of Zoology, University of Michigan, No. 53. University of Michigan Press. Ann Arbor. 128 pp.

Rossi, L. and A.E. Fano. 1979. Role of fungi in the trophic niche of the congeneric detritivorous Asellus aquaticus and A. coxalis (Isopoda). Oikos 32:380-385.

Rossi, L. and G. Vitagliano-Tadini. 1978. Role of adult faeces in the nutrition of larvae of Asellus aquaticus (Isopoda). Oikos 30:109-113.

Rounick, J.S. and M.J. Winterbourn. 1983. The formation, structure and utilization of stone surface organic layers in two New Zealand streams. Freshwater Biology 13:57-72.

Saunders, G.W. 1980. Organic matter and decomposers, pp. 341-392. In: E.D. LeCren and R.H. Mcconnell, eds. The