J. N. Am. Benthol. Soc., 1986, 5(3):200-210 O 1986 by The North American Benthological Society Feeding behavior of interpunctatum (Ephemer0ptera:)

D. MCSHAFFREYAND W. P. MCCAFFERTY Department of Entomology, Purdue University, West Lafayette, Indiana 47907 USA

Abstract. Larvae of (Ephemer0ptera:Heptageniidae) were observed feed- ing under naturalistic conditions using macroscopic video techniques. The stereotypic feeding behavior is depicted as a cycle consisting of stages of coordinated movement of the entire suite of mandibulate mouthparts. Depending on experimental conditions this behavioral cycle was modi- fied to enable individuals to brush loosely accreted material from the substratum, gather detritus from deposits, or passively filter detritus from the current. Larvae were most successful in feeding on loose particles of detritus. When presented with attached algae, larvae would attempt to brush the material from the substratum using the labial and maxillary palps with little success in remov- ing tightly accreted material. Feeding observations combined with field and laboratory data on gut content and microhabitat distribution data suggest that S. interpunctatum larvae are opportunistic collectors (gatherers). Key mords: Ephemeroptera, Heptageniidae, Stenacron interpunctatum, feeding behavior, morphology, ecology.

An important aspect of any 's ecology subject of the research reported here, have been is its role as a consumer. In freshwater ecology, placed in a "scraper" functional category by particularly in studies of running water, the Cummins et al. (1984), defined as consisting of consideration of feeding relationships of ben- organisms feeding on "attached algae and as- thic macroinvertebrates has been crucial to sociated material" (Cummins and Merritt 1984). conceptualizing community dynamics and pre- "Gatherers", defined as organisms that collect dicting ecological relationships (Cummins 1973, detritus from sedimentary deposits, is another 1974, Vannote et al. 1980). Despite the funda- functional category in which Stenacron was mental importance of such information, feed- placed (Cummins et al. 1984). Other authors ing habits are often inferred from reports of have defined these groups differently; for ex- similar taxa because most species have not re- ample, Lamberti and Moore (1984) broaden the ceived critical autecological study. Conclusions definition of scrapers to include organisms that about feeding have usually been based on gut collect material other than algae from crevices content analyses and casual observations. Un- in the substratum. fortunately, gut contents can be misleading be- We have studied the functional feeding role cause of seasonality and errors introduced in of Stenacron interpunctatum by analyzing func- sampling, dissection, and identification of par- tional morphology and feeding behavior. This tially digested material (Shapas and Hilsenhoff approach allows us to define more accurately 1976). It may not be clear which material in the the feeding role of the animal, and also to make gut is nutritionally important. Casual observa- informed estimates about the functional roles tions of behavior can seriously underestimate of other organisms with similar morphology. the complexity of an organism's feeding activ- Other studies of have combined ob- ities. servation and morphological analyses (Brown Perhaps the most difficult task in organizing 1960, 1961, Froehlich 1964, Rawlinson 1939, feeding ecology data is the grouping of organ- Schonmann 1981, Strenger 1953, 1975). Our isms into categories descriptive of similar feed- study, however, differs considerably by incor- ing habits. Classifications based on food types porating a recording device for detailed mo- are the oldest. Cummins (1973), however, has tion analyses, scanning electron microscopy argued for the need of categories based on (SEM) for analysis of fine structure and topol- functional characteristics. As an example, lar- ogy, and novel viewing angles. In addition, our vae of the genus Stenacron, which is the primary observation system was designed to 19861 FEEDINGIN STENACRON INTERPUNCTATUM 201 duplicate natural stream conditions (i.e., flow, filters transmit less than 0.1% of the light below light levels, orientation) more closely than the 780 nm, the LEDs transmit at 880 nm; thus the studies cited above. light used was essentially non-visible to hu- We have chosen S. interpunctatum as our pro- mans. High reflectiveness by Stenacron eyes and totypic subject because it is common in the the lack of observed responses to changes in eastern half of North America and easily cul- infrared light intensity indicated that the in- tured. Furthermore, mature larvae are large frared light sources were non-visible to the enough (head capsule width >2.5 mm) to ob- study organisms. Other observations were car- serve with ease, and individuals continue to ried out under visible light which allowed feed even under the high illumination often smaller lens diaphragm openings to be used, required for documentation. We view this study thus increasing resolution and depth of field. as ecologically important because Stenacron and A variety of lenses and lens extensions were its relatives in the family Heptageniidae are employed to allow magnification up to 80 x on often important or even dominant in certain a 9" (23 cm) high resolution black and white lotic habitats (Bednarik and McCafferty 1979). video monitor. A %" (12.7 mm) VHS format Our objectives in this study were to document Panasonic NV-8950 video recorder with freeze- the feeding behavior of S. interpunctatum and frame, slow motion, and reverse option capa- identify the structures used in feeding. Because bilities allowed images to be recorded and ana- this study is part of a larger, comparative in- lyzed. vestigation of the feeding behavior and asso- A larva was placed for observation in a cell ciated morphology of larval mayflies, we have built of %" (12.7 mm) thick clear acrylic (Fig. deferred critical study of the nutrition of this I), having a 1 x 3-cm rectangular depression in species, and we have not attempted to prepare the center. Several cells were constructed with a complete ethogram of its behavioral reper- depths ranging from 1 to 5 mm. At each end toire. of the depression several small holes were drilled down into the material to join with larger holes leading out to the edge of the Methods acrylic. Aquarium tubing was cemented into Organisms were collected from early spring these larger holes. The depression was sur- to late fall from cobble substrate in the Tippe- rounded with self-adhesive automotive gasket canoe River in north-central Indiana, and were material and covered with a 75 x25-mm glass maintained in the laboratory in large aquaria microscope slide. The slide was held in place filled with substratum and water from the col- by a second piece of clear acrylic, %'I (6.35 mm) lection site. Circulation in the aquaria was pro- thick, that had its center removed to corre- vided by airstones placed on the bottom. Only spond with the depression; this hole was also large (head capsule width >2.5 mm) larvae were surrounded by gasket material. The apparatus used for observation and videotaping. was held together by bolts inserted through Individuals were observed by the following holes in both pieces and secured with wing techniques. Initially, to minimize possible dis- nuts. The observation cell was placed in the tractions, individuals were observed in a large theater with the long axis in a vertical position light-proof observational theater insulated to and the glass slide facing the camera. The stage reduce sound vibrations. The observer was out- on which the cell was mounted was moved in side the theater, and by remote control oper- three axes by electric motors. ated the video camera (Panasonic WV-1850 with Water at room temperature (20°C) was cir- 1" Extended Red Newvicon S4119 pickup tube) culated through the cell by pumping or si- mounted inside the theater for observation. The phoning it into the cell through the lower tube theater and monitoring system, which were de- and out the upper. The flow was controlled by signed for a study of burrowing behavior, were a valve; however, current velocities around the described in more detail by Keltner and Mc- larva (as measured by timing the movement of Cafferty (1986). Light was provided either by small particles) varied even within a given ex- an externally mounted fiber optic illuminator periment. The larva could occupy a significant equipped with Kodak Wratten No. 87c filters portion of the cross-sectional space within the or by infrared light-emitting diodes (LEDs). The shallowest observation cells; this had a dynam- D. MCSHAFFREYAND W. P. MCCAFFERTY [Volume 5

TOP VIEW

FIG. 1. Observation cell used for observations of feeding behavior in mayfly larvae, drawn to scale. Unlabelled arrows indicate direction of water flow. Abbreviations: BH = Bolt Hole, BP = Base Plate, BS = Base Support, CB = Clamp Bolt, EC = Excavated Chamber, EO = Experimental Organism, FC = Flow Colli- mator, FP = Face Plate, GA = Gasket, MS = Microscope Slide, VP = Viewing Port, WT = Water Tubing. 19861 FEEDINGIN STENACRON INTERPUNCTATUM 203 ic effect on local current velocities and pro- mouthparts. For our purposes the stages are de- duced a complicated pattern of streamlines of lineated by changes in the movements of the varying current velocities within the cell. For labium and the labial palps. most experiments flow was adjusted until the Additional observations were made of or- larva began to orient. This adjustment was nec- ganisms on more natural substratum in aquaria essary because of the difficulty in measuring and in small artificial streams to assess the effect current velocity (or deciding which velocity was of the theater and observation cell on behavior, significant to the organism). Orientation usu- and to check the accuracy of the descriptions ally occurred at "low" current velocities (0-5 of the feeding cycles. These observations were cm/s). made by eye, with and without a stereomicro- Food was introduced into the observation cell scope, and with the video camera. These meth- by several means. Algae taken from the Tip- ods did not provide the detail and/or repeat- pecanoe River were cultured in the laboratory ability necessary for critical analysis of directly on the glass slide forming the viewing mouthpart movement; however, resolution is wall of the observation cell. The slides were greater during the initial, direct observation covered primarily (95%) with Cocconeis; bacte- than on videotape playback. We have found ria were common between these diatoms. The this also to be true for the species of mayflies remaining 5% was covered by scattered fungal and other aquatic invertebrates that have or are hyphae, Oscillatoria, Cladophora, Melosira, Fragil- being studied using similar techniques. laria, Chlorella, rotifers, and protozoa. Slides Mouthpart structures were examined by light were examined microscopically before and af- microscopy and SEM. This information was ter the observation period. Feeding was consid- used to construct a moveable plastic model of ered effective if the slides contained patches the mouthparts to aid further understanding of where the algae had been removed, or if actual their motion. removal and ingestion were observed. Detritus Gut contents of living larvae were placed on taken from the holding tanks was placed in the glass microscope slides and examined imme- cell and feeding was observed at low and high diately with a compound microscope. Gut con- flow rates. Feeding on detritus was considered tents of individuals freshly collected in the field effective if ingestion was observed. were compared to those held in the laboratory. Motion analyses were carried out primarily Gut contents were classified as being mineral, by examination of the videotape recordings of organic detritus, diatoms, filamentous algae, the observation sessions of the organisms in unicellular algae, animal remains, or bacteria. the cells; however, this was supplemented by No attempt was made to quantify proportions direct video observation. Over 20 individuals other than to note what type predominated. of S. interpunctaturn were observed for a total period of over 50 hours in the course of this Results study. Ten of these individuals were video- Field observations taped in the observation cells; 236 feeding cycles from eight of these individuals (four lar- The open canopy at the collection site per- vae feeding on attached algae and four larvae mitted algal growth to cover the substratum. feeding on detritus) were analyzed in detail The aufwuchs community was more diverse using the single frame advance feature of the than that cultured on slides in the laboratory. videotape recorder. This information was used Additional taxa of diatoms such as Gomphone- to assemble a chronology of mouthpart move- ma, Gyrosigma, Nauicula, and Synedra were also ments which was checked against the remain- present. Certain taxa such as Cladophora, Melo- ing videotape. In all, several thousand feeding sira, and Fragillaria had seasonal blooms to a cycles were examined. Following the protocol point where they visibly dominated the pe- of Keltner and McCafferty (1986), the observed riphyton community. At times large areas of feeding behavior was classified into stereotypic the substrate were covered by blackfly larvae cycles describing different methods of obtain- and pupae, or by the silk retreats of Petrophila ing and handling possible food material. Each (Lepidoptera) or chironomid larvae. cycle was divided into stages to describe the The larvae collected in the field were, with- choreography of movement of the suite of out exception, collected from the bottoms of D. MCSHAFFREYAND W. P. MCCAFFERTY [Volume 5

lingua of denticles of mandible mOla of

basal segment of

of labium

prementum basal segment of labial palp FIG. 2. Ventral view of the mouthparts of Stenacron interpunctatum. Mouthparts have been moved from the resting position to allow underlying structures to be seen. stones. Although sampling was not quantita- by external stimuli ceased after 1-2 cycles of tive, comparable numbers of S. interpunctatum the mouthparts; those that appeared to be in- larvae were found among the cobble substra- duced by the organism typically continued for tum both in the open canopy areas and under at least 5 cycles. Feeding movements observed an adjacent highway bridge where shading vis- under visible light were identical to those ibly reduced algal growth. Larvae were more viewed with infrared light. Specimens ob- commonly collected from areas of slower cur- served in the artificial streams and holding rent. aquaria were negatively phototactic, positively thigmotactic and positively rheotactic. Effects of experimental conditions on behavior Stereotypic feeding behavior Mature larvae of S. interpunctatum were high- ly stereotypic in the movement of their mouth- Resting position. When a larva is not feed- parts in all experimental enclosures (observa- ing, its mouthparts (Figs. 2,3,4a-e) are held in tion cells, artificial streams, holding aquaria a characteristic resting position (Fig. 5a). The with natural substratum). The few variations in distal segment of the labial palps are held fold- feeding movements observed were apparently ed inward so that they lie over the glossae and associated with food type and are described be- paraglossae. The labium as a whole is held ad- low. In every case, movements were indepen- ducted dorsally to close the preoral cavity ven- dent of experimental enclosures. trally. The galealaciniae of the maxillae are po- External factors such as noise, vibration, sitioned with their median setae touching the changes in visible light intensity or water ve- lingua of the hypopharynx; the galealaciniae locity did not affect the qualitative perfor- also are in contact ventrally with the labial palps mance of feeding movements of S. interpuncta- and dorsally with the superlinguae of the hy- turn. They did, however, affect the duration of popharynx. The distal segments of the maxil- movements and the release of stereotypic feed- lary palps are held folded over the anterior ing movements. Feeding movements induced opening of the preoral cavity. The mandibles FEEDINGIN STENACRON INTERPUNCTATUM 205

head capsule

suwrl!ngua

galealannla labral palp

VENTRAL FIG. 3. Diagrammatic cross-section of the mouth- parts of S. interpunctatum, showing relative vertical positions. are held with the denticles separated, and the molae presumably closed. The labrum is held pressed against the head capsule dorsally and the mandibles ventrally. Brushing cycle. A larva placed in the obser- vation cell with algae grown on the glass slide performed a behavioral cycle we term brush- ing. A brushing cycle comprises several stages delineated by the movements of the labium. A single brushing cycle, as described below, takes FIG. 4. Ventral view of mouthparts of Stenacron approximately 1 second at 20°C. The mouthpart interpunctatum, ventral to dorsal sequence. a. Labium. movements described below are often preced- b. Maxillae. c. Hypopharynx. d. Mandibles. e. La- ed by vigorous movement of the forelegs ahead brum. (upstream) of the individual. The legs are re- peatedly extended and then retracted, drawing the claws over the substratum; this movement distal segments of the labial palps are abduct- ceases during the first cycle. We did not find ed, moving through a range of about 30". As any evidence that such movement of the fore- the apical tips of the labial palps clear the glos- legs displaces material adhering tightly to the sae and paraglossae, the labium completes its substrate. ventral swing coming to rest against the sub- Stage 1.-Abduction of the basal segments of stratum with the labial palps fully extended, the labial palps: As feeding commences, the la- yet remaining under the contour of the head bium begins to swing ventrally towards the capsule (Fig. 5c). At this point the galealaciniae substrate. The basal segments of the labial palps are abducted, moving laterally outward. The swing posteriorly about 10" (Fig. 5b); this maxillary palps have been extended and reach movement partially displaces the distal seg- beyond the lateral borders of the head capsule. ments of the labial palps from contact with the The denticles of the mandibles begin to move glossae and paraglossae. At this point the basal laterally outward. The labrum completes its segments of the maxillary palps swing poste- movement posteriorly and ventrally, effective- riorly. The galealaciniae do not move in Stage ly shielding the mouthparts under the head 1 of the first brushing cycle, but in all subse- capsule from the current. quent brushing cycles they move medially at Stage 3.-Retraction of the labial palps: The this point. The labrum begins to move down labial palps are retracted from their extended and backwards to shield the front of the other position by a combination of an anterior swing mouthparts. of the basal segments of the palps and adduc- Stage 2.-Abduction of the distal segments of tion of the distal segments of the palps. This the labial palps: Once the basal segments of the movement is continuous and coordinated so labial palps reach their posterior position, the that the palps always remain under the head 206 D. MCSHAFFREYAND W.P. MCCAFFERTY [Volume 5

movement and the maxillary palps are inserted among these denticles (Fig. 5e). The labrum moves dorsally. As feeding continues, this brushing cycle is repeated with the abduction of the basal seg- ments of the labial palps as in Stage 1 (foreleg movement is not repeated). The brushing cycle is repeated unchanged except that in Stage 1of subsequent cycles the galealaciniae are adduct- ed medially, and the posterior movement of the basal segments of the maxillary palps draws the apical setae of the maxillary palps through the combs on the denticles of the mandibles. Gathering cycle. When S. interpunctatunz is presented with loose detritus, a gathering cycle is performed. The gathering cycle is similar to the brushing cycle except for the following. The mouthparts are not pressed tightly against the substratum in Stage 2, and the legs, particularly the forelegs, may bring detritus to the preoral cavity where it is swept up by the labial palps as they move inward in Stage 3. The lateral setae on the distal segments of the labial palps carry more material from the substratum than FIG.5. Relative positions (all in ventral view) of the ventral setae. In Stage 3 the apical setae of the mouthparts of Stenacron interyunctntum during the maxillary palps bring a larger volume of various stages of the brushing feeding cycle. a. La- detritus to the preoral cavity than in the brush- bium and maxillae, resting position. b. Labium and ing cycle; this material is combed out by the maxillae, Stage 1 of initial cycle. c. Labium and max- mandibular denticles when the maxillary palps illae, Stage 2. d. Labium and maxillae, Stage 3. e. are withdrawn in Stage 1. Maxillae, hypopharynx and mandibles, Stage 3. f. When presented with filamentous algae such Maxillae and hypopharynx, Stage 1 of subsequent cycles. as Cladophora sp., the mouthparts are posi- tioned in Stages 2 and 3 so that the labial palps brush over the filaments, removing epiphytes. capsule. As the distal segments of the labial The maxillary palps play a role in manipulat- palps move they brush (sweep) up material ing the filaments. It is possible for the organ- from the substratum with the profuse setae on ism to manipulate filaments into the preoral the ventral and anterior surfaces. When the cavity; however, what could be interpreted as distal segments of the labial palps reach the attempts to bite off and swallow pieces of such paraglossae they are raised dorsally by a rota- filaments were ineffective. tion of the basal segments of the palps so that Filtering cycle. When a heavy load of detri- they pass dorsal to the paraglossae and glossae. tus is moving in the current, S. interpunctatum The distal segments of the palps reach a posi- alters its feeding behavior radically and be- tion that is more median than in the resting comes a passive filter feeder. The filtering cycle position (Fig. 5d). The entire labium is raised is less complex than the other cycles, and the as soon as the distal segments of the labial palps labial palps are not used to gather food. The are dorsal to the glossae and paraglossae. The larva orients so that its head faces into the cur- galealaciniae follow the labial palps in moving rent and the longitudinal axis of the body is medially; they also move somewhat ventrally. parallel to the flow. The mouthparts are held The maxillary palps sweep inward, brush over in the resting position except for the maxillary the substratum, and enter the preoral cavity palps; these are extended until they are per- dorsal to the superlinguae. The denticles of the pendicular to the flow. Particles of detritus ad- mandibles complete their lateral outward here to the apical setae. Periodically the max- 19861 FEEDINGIN STENACRONINTERPUNCTATUM 207 illary palps are retracted into the preoral cavity bears rows of setae on its dorsum which guides as in Stage 3 of the brushing cycle. The detritus the material to a point where it can be pressed brought to the preoral cavity is combed out from against the mandibular molae for straining and the apical setae of the maxillary palps by the ingestion. Presumably, material left on the denticles of the mandibles as in Stage 1 of the denticles is brushed directly onto the dorsum brushing and gathering cycles; the detritus is of the hypopharynx by movements of the man- then further processed in the manner de- dibles; we have not been able to observe this scribed below, except that the labial palps do since this area is obscured by the other mouth- not gather additional food. parts. The maxillary palps are used in all cycles to displace larger particles from the preoral cavity Food processing and to brush material from the comb setae on Once food material has been acquired by the the galealaciniae. Once food acquisition ceases, palps of either the labium or the maxillae in the mouthparts (except for the labial palps) re- any of the cycles above, it must be positioned main in motion as described above for several for ingestion. This process is carried on contin- cycles, moving material into position to be in- uously during feeding and for several seconds gested. after the last material is acquired from the sub- stratum. The transfer is accomplished by suc- Gut content analysis cessive fields of setae on the various mouth- Organisms collected in the field had little va- parts (Fig. 2) as described below. riety in their gut contents. All guts contained After completion of at least one brushing or mineral material and organic detritus. Diatoms gathering cycle, and when the labial palps are were observed in the gut of only a few indi- extended again (Stage I), the material on their viduals collected early in November 1985,when setae is removed in two ways. The outward lat- a dense growth of diatoms, predominately eral movement (Stage 1) of the distal segments species of Melosira and Fragillaria, covered the of the labial palps causes material to be combed substratum in the Tippecanoe River. Whereas from the ventral setae of the labial palps by the some of these diatoms were present in the gut, setae on the dorsal surfaces of the glossae and they were not predominant, and the diatom paraglossae. Material on the lateral setae of the frustules were intact. None of the larvae col- distal segments of the labial palps is removed lected in the field had filamentous algae, uni- by the comb setae of the galealaciniae as they cellular algae, or animal remains in their guts. move medially in opposition to the outward Individuals held in the lab had gut contents movement of the labial palps (Stage 1).The ma- similar to those newly collected in the field, terial in the comb setae is brushed out as these although some of the individuals held in the setae are drawn base-first through the setae on laboratory did contain the diatom Cocconeis sp. the glossae and paraglossae by the ensuing out- ward lateral movement of the galealaciniae Discussion (Stage 2). In all cycles, material on the maxillary palps In any behavioral study, it is important to is removed by the combs on the mandibular assess the impact of experimental protocol on denticles as the palps are withdrawn (Stage 2). behavior. In our study the need to confine the In the filtering cycle all material is brought to organisms to a small area to allow for high the mouth in this way. magnification observation required an enclo- Material left on the glossae and paraglossae sure that did limit the overall behavior of the is moved further through a number of process- organism. Since our objective was only to doc- es. As the labial palps return to the preoral cav- ument a small portion of the species' overall ity (Stage 3), this material is displaced poste- behavioral repertoire, this limitation was not a riorly, medially, and dorsally by the palps and significant constraint because the portion of the the new load of material they bear. As the ga- behavior in which we were interested was not lealaciniae move medially (Stage l), their me- affected. The brushing cycle and the gathering dian setae push the material between the su- cycle were performed in an identical fashion perlinguae and the lingua (Fig. 5f). The lingua in the observation cell, in aquaria, and in the 208 D. MCSHAFFREYAND W. P. MCCAFFERTY [Volume 5

artificial stream. Our observations of other marily ingest detritus (Lamp and Britt 1981), Ephemeroptera, Trichoptera, Diptera, Odonata, the importance of this food source in the diet Coleoptera, Amphipoda, Gastropoda, and other of this species is significant. freshwater macroinvertebrates suggest that the The ability of S. interpunctatum to vary its cyclic movements of the mouthparts are stereo- feeding behavior to either filter or gather de- typic and vary little if any between individuals pending on the circumstances demonstrates its of the same age class of any one species. This independence from a single resource such as conclusion is consistent with other feed- periphyton. A more tenable classification of S. ing studies (Brown 1960, Chance 1970, Devitt interpunctatum as primarily a collector has im- and Smith 1985, Froehlich 1964, Pucat 1965). portant consequences for ecological investiga- This study shows that S. interpunctatum is an tions incorporating or extrapolating from the opportunistic feeder with a behavioral reper- river continuum concept. toire sufficient to allow it to feed in a number On the basis of their mouthpart structure, of different ways. The importance of detritus heptageniids, in general, have sometimes been as a food source for this species has been doc- assumed to scrape their food. For example, umented by Lamp and Britt (1981); their quan- Brown (1960) wrote that the crown setae of the titative gut content data agree with our quali- maxillae are used to rake up diatoms; however, tative observations. Our laboratory observations this statement actually was a misinterpretation combined with ecological observations from the of Strenger (1953) (in German) who described field suggest that this species is better classified the function of these setae ("Kammborsten") as as a collector-gatherer than as a scraper accord- combs for the labial palps. We found that the ing to the categories of Cummins and Merritt orientation of these setae aligns them precisely (1984). In laboratory tests S. interpunctatum was with the labial palps, and that they cannot reach not able to remove tightly adhering diatoms the substratum because of the position of the such as Cocconeis sp. from a glass slide; how- large labium between the maxillae and the sub- ever, individuals on more natural substrata are stratum. The external chitinized "scraping bars" apparently able to remove this diatom to some reported by Morgan (1911) on the distal seg- extent. The only alga that S, interpunctatum was ments of the labial palps in the heptageniid observed to ingest was an extremely flocculent Epeorus fragilis are not present in S. interpunc- mass of diatoms with physical characteristics tatum. Examination of the distal segments of similar to loose detritus. Although the organ- the labial palps of S. interpunctatum by light mi- isms are capable of manipulating filamentous croscopy revealed structures which could be algae and removing epiphytes from surfaces of interpreted as scraping bars, but examination these plants, they have difficulty biting off sec- with SEM revealed that they were internal tions of the filaments. Filamentous algae, structures (probably apodemes). Further inves- however, have been reported in the gut of Ste- tigations will be needed to see if this is not the nonema modestum, a closely related and mor- case for other heptageniids. phologically similar species (Kondratieff and The only mouthparts of S. interpunctatum that Voshell 1980). reach the substratum are the labial palps and Microhabitat data also suggest that this the tips of the maxillary palps. Both of these species is a collector-gatherer. We consistently structures are heavily setose and not fit for found these larvae on the undersides of stones scraping in the manner we have observed for in crevices where detritus was deposited. Oth- radulae of gastropods and the mandibles of er studies (Wiley and Kohler 1980, Wodsedalek water penny beetle larvae (Psephenus).We have, 1912) also stressed the occurrence of S. inter- however, seen the heptageniid Heptagenia pa- punctatum larvae on the undersides of stones. vescens scrape bacterial film from the substra- Although direct observation and analysis of tum. The terminal ends of the maxillary palps feeding behavior of earlier instars of S. inter- of that species are reinforced and modified as punctatum were not conducted in this study, a scraping tool, quite unlike the brush-like earlier instars of many species may be detriti- maxillary palps of S. interpunctatum. It is possi- vores even if they later specialize on other food ble that the forelegs of S. interpunctatum may be sources (Cummins 1973, Cummins and Merritt capable of some scraping. They are active be- 1984).Since mature S. interpunctatum larvae pri- fore the brushing cycle and are important in bringing food to the mouth in the collecting (Ephemer0ptera:Heptageniidae). Canadian Bul- cycle. The fact that we did not observe them to letin of Fisheries and Aquatic Sciences 201:l-73. be effective in removing material from the sub- BROWN,D. S. 1960. The ingestion and digestion of stratum may be an experimental artifact. algae by Cloeon dipterum L. (Ephemeroptera). Hy- drobiologia 16:81-96. From a functional-morphological stand- BROWN,D. S. 1961. The morphology and function point, it is desirable to erect a new category of of the mouthparts of Cloeon dipterum L, and Baetis feeding-'brushing'-distinguished from rhodani (Pictet) (Insecta, Ephemeroptera). Pro- scraping by the morphological structures used ceedings of the Zoological Society of London 136: in acquiring material from the substratum. We 147-176. propose that brushers include organisms that CHANCE,M. M. 1970. The functional morphology remove material from the substratum using se- of the mouthparts of black fly larvae (Diptera: tae, and that scrapers include organisms that Simuliidae). Quaestiones Entomologicae 6:245- use hardened structures such as mandibles or 284. radulae to remove accreted material. Whereas CUMMINS,K. W. 1973. Trophic relations of aquatic . Annual Review of Entomology 18:183- such a distinction is valuable from a functional 206. standpoint, its ecological significance may be CUMMINS,K. W. 1974. Structure and function of less apparent and awaits data about what pre- stream ecosystems. BioScience 24:631-641. cise components of the aufwuchs can be re- CUMMINS,K. W., G. F. EDMUNDS,AND R. W. MERRITT. moved by each of these functions and what 1984. Summary of ecological and distributional components are nutritionally significant. data for Ephemeroptera (mayflies). Table IOA, Analyses of the feeding behavior and func- pages 122-125 in R. W. Merritt and K. W. Cum- tional morphology of a species are important mins (editors).An introduction to the aquatic in- tools in describing the ecological relationships sects of North America. Kendall-Hunt Publish- of that species. Such studies are necessary be- ing Company, Dubuque, Iowa. CUMMINS,K. W., AND R. W. MERRITT.1984. Ecology fore ecological assumptions based on morphol- and distribution of aquatic insects. Pages 59-65 ogy are made, and provide additional insight in R. W. Merritt and K. W. Cummins (editors). into the relevance of gut content data. As more An introduction to the aquatic insects of North of these studies are completed within taxonom- America. Kendall-Hunt Publishing Company, ic groupings and among taxa with similar mor- Dubuque, Iowa. phology their usefulness will increase as an aid DEVITT,B. D., AND J. J. B. SMITH. 1985. Action of in understanding community dynamics and mouthparts during feeding in the dark-sided evolutionary trends. cutworm, Euxoa messoria (Lepid0ptera:Noctui- dae). Canadian Entomologist 117:343-349. FROEHLICH,C. G. 1964. The feeding apparatus of the Acknowledgements nymph of Arthroplea cogener Bengtsson (Ephem- eroptera). Opuscula Entomologica 29:188-208. We thank John Keltner for his technical as- KELTNER,J., AND W. P. MCCAFFERTY.1986. Function- sistance and advice; Arwin Provonsha, whose al morphology of burrowing in the mayflies illustrations translate complex three-dimen- Hexagenia limbata and Pentagenia vittigera. Zoolog- sional relationships to the two-dimensional ical Journal of the Linnean Society 87:139-162. world of the journal page; and Dan Bloodgood KONDRATIEFF,B. C., AND J. R. VOSHELL.1980. Life for assisting with field work, construction of history and ecology of Stenonema modestum the observation cells, and preparation of Figure (Banks) (Ephemer0ptera:Heptageniidae) in Vir- 1.The scanning electron microscope was made ginia, USA. Aquatic Insects 2:177-189. available by the Electron Microscopy Center in LAMP,W. O., AND N. W. BRITT. 1981. Resource par- titioning by two species of stream mayflies Agriculture at Purdue University with support (Ephemer0ptera:Heptageniidae). Great Lakes from NSF grant PCM-8400133. Entomologist 14:151-157. Purdue University Agricultural Experiment MORGAN,A. H. 1911. Mayflies of Fall Creek. Annals Station Journal No. 10,178. of the Entomological Society of America 4:93- 119. Literature Cited PUCAT,A. M. 1965. The functional morphology of the mouthparts of some mosquito larvae. Quaes- BEDNARIK,A. F., AND W. P. MCCAFFERTY.1979. Bio- tiones Entomologicae 1:41-86. systematic revision of the genus Stenonema RAWLINSON,R. 1939. Studies on the life-history and 210 D. MCSHAFFREYAND W. P. MCCAFFERTY [Volume 5

breeding of Ecdyonurus venosus (Ephemeroptera). Sowa (editors). Proceedings of the 2nd Interna- Proceedings of the Zoological Society, Series B: tional Conference on Ephemeroptera (1975). 377-450. VANNOTE,R. L., G. W. MINSHALL,K. W. CUMMINS,J. SCHONMANN,H. 1981. Zur Kopfmorphologie der R. SEDELL,AND C. E. CUSHING.1980. The river Ephemeridenlarven Siphlonurus aestivalis Eaton continuum concept. Canadian Journal of Fish- und Lepeorus goyi goyi Peters. Zoologica (Stutt- eries and Aquatic Sciences 37:130-137. gart) 131:l-51. WILEY,M. J., AND S. L. KOHLER.1980. Positioning SHAPAS,T. J., AND W. L. HILSENHOFF.1976. Feeding changes of mayfly nymphs due to behavioral habits of Wisconsin's predominant lotic Plecop- regulation of oxygen consumption. Canadian tera, Ephemeroptera and Trichoptera. Great Lakes Journal of Zoology 58:618-622. Entomologist 9:175-178. WODSEDALEK,J.E. 1912. Natural history and general STRENGER,A. 1953. Zur Kopfmorphologie der behavior of the Ephemeridae nymphs Heptagenia Ephemeridenlarven. I. Teil Ecdyonurus und interpunctata. Annals of the Entomological Soci- Rhithrogena. Osterreichische Zoologische Zeit- ety of America 5:31-40. schrift 4:191-228. STRENGER,A. 1979. Die Ernahrung der Ephemer- Received: 15 May 1986 opterenlarven als funktionsmorphologisches Accepted: 22 September 1986 Problem. Pages 299-306 in K. Pasternak and R.