movement patterns and foraging ecology of a stream caddisfly larva

Movement patterns and foraging ecology of a stream caddisfly larva

DAVID D. HART' Division ofEnvironmenta1 Studies and Ecology Graduate Group, University of California, Davis, CA, U.S.A. 95616

A N D

VINCENT H. RESH Division of Entomology and Parasitology, University of California, Berkeley, CA, U.S.A. 94720

Received August 21, 1979

HART. D. D., and V. H. RESH. 1980. Movement patterns and foraging ecology of a stream caddisfly larva. Can. J. Zool. 58: 1174- 1185.

The movement patterns and time-activity budgets of Dicosmoecus gilvipes were quantified from underwater observations of marked individuals in a northern California stream, during two studies in early and late June, 1977. Individuals traveled several metres per day. The only striking differences between the observed patterns of movement and those predicted from a random walk model are the following: ( a ) in both studies, large larvae moved significantly farther than small larvae; (b) in both studies, there is apronounced die1 rhythm to movement, with animals traveling faster during the day; ( c ) rates of travel In late June are -3 times faster than those in early June. Since more than two-thirds of the total time-activity budget of these larval insects is dedicated to feeding, we suggest that the patterns of movement reported here largely reflect activities related to food acquisition. Several observations indicate that food is locally limiting and heterogene- ously distributed across the stream bottom, thus requiring animals to move from patch to patch in order to meet their food requirements. Seasonal differences in rates of movement appear to result from phenological changes in the quantitative and qualitative food requirements of these stream insect grazers.

HART, D. D., et V. H. RESH. 1980. Movement patterns and foragingecology of a stream caddisfly larva. Can. J. Zool. 58: 1174-1 185.

Cette etude a pour but de quantifier les mouvements et le temps consacre aux activites de Discosmoecus gilvipes; des specimens ont donc e t t marques et observes sous l'eau, dans un ruisseau du nord de la Californie, durant deux pkriodes, au debut et a la fin de juin 1977. Les larves se dcplacent de plusieurs metres par jwr. Les seutes differences marquees entre les patterns des mwuvements observis et ceux qui ont ett privus d'apres un modele de marche albtoire sont les suivants: {oldurant lcs deux htudes. Ies larvcs degrandc taille vont significativement plus loin que les petites Iarues, ( h ) doran! les deux irudes. l'activit6 suit un rythme juurnalier marque. puisque les larveq se deplaccnt beaucoup plus rapidement duranr le jour et I r . ) la vitcsse de diplacement est envimn tzois fois plus rapide i la fin de juin qu'au dkhut de juin. Les lames accordent plus des deux tiers de leur temps d'activitk a I'alimentation; il est donc Itgitime de croire que les diplacements observes refietent en grande, panie des activitis relikes a la recherche de no&- turc. Plusieurs observations indiquent que I'alimcntation impose une contrainte spatiale. puisque la nourrirure est rkpartie de far;un hitkmgknc sur le substrat; les larves doivent donc se deplacer d'une source de nnurriture i une autre pour repundre a Ieurs besoins alirncntaires. Les variations saisonnicres de la vitcsse de deplacement sernhlent reliies ades changements phPnologique5 des besoins alimentaires quantitatifs et qualitatifs de ces larves "brouteuses."

[Traduit par le journal]

Introduction The movement of animals within and between

habitats is of particular ecological significance. Patterns of movement, whether associated with long-range migrations or a localized search for shelter, food, mates, or other factors, provide an index of an organism's perception of environmental grain (Levins 1968; Wiens 1976). In many cases, the degree to which an animal is sedentary or mobile has a clear adaptive basis, and it seems likely that

'Present address: W. K. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, U.S.A. 49060.

studies of mobility will aid in the development of conceptual models linking the behavioral ecology of animals with the patchiness of their environments.

This study considers patterns of movement in the larval stage of Dicosmoecus giluipes Hagen (Trichoptera: Limnephilidae), a stream caddisfly. Previous studies of stream benthic invertebrate behavior can generally be placed in one of three categories: (1) the study of invertebrate drift, in which animals move downstream with the current as a result of either active or passive processes (see reviews of Waters 1972; Miiller 1974; Adamus and

0008-4301/80/061174-12$01 .W/O 01980 National Research Council of Canada/Conseil national de recherches du Canada

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HART AND RESH 1175

Gaufin 1976); (2) analyses of upstream movements, a phenomenon thought by some to counteract the tendency of animals to be displaced downstream as a result of drift (e.g., Bishop and Hynes 1969; Hul- tin et al. 1969; Elliott 1971; Luedtke and Brusven 1976; Williams and Hynes 1976); (3) laboratory studies of die1 rhythms in locomotion and other behavior (e.g., Elliott 1969, 1970; Thorne 1969; Lehmann 1972; Gallepp 1974).

The approach taken here differs in several re- spects from previous behavioral studies of invertebrates in streams. Because of our interest in the relationship between movement and the heterogeneity of the natural environment, this study was conducted in the field. Thus, a marking and sampling method was developed in order that the movements of individual larvae could be easily fdlowed in their natural habitat. Although various methods have been used to mark stream invertebrates as a group (e.g., Harker 1953; Lehmann 1964; Elliott 1969, 1970; Thorne 1969; Brusven 1970; Gallepp and Hasler 1975), these have seldom been applied to field studies, and no studies exist which follow the movements of individually marked animals. Furthermore. in only one study (Gallepp and Hasles 1975) have investigators at- tempted to directly assess whether the marking method alters behavior.

The objectives of this study are as follows: (1) to evaluate the effect of marking on larval behavior in order to determine whether data gathered from tagged individuals can be realistically generalized to the population as a whole; (2) to describe the distance and direction patterns of larval movement, and to compare statistically the observed patterns with those expected on the basis of random movement; (3) to consider the possible influence of environmental patchiness on larval movement, and thereby evaluate alternate hypotheses regarding the adaptive significance of these movement patterns.

Life history overview Dicosmo~cus gilvipes is a unjvoltine species with

a single larval cohort. AduIts fly in September and October, and individuals overwinter as early larval instars. By late April, second, third, and fourth instars predominate. In early July a11 larvae have reached the final (fifth) instar, after which individuals enter a prepupal resting stage lasting from 1 to several weeks. Pupation follows, and emergence begins in late summer.

The larvae of D. gilvipes gather most of their food by grazing periphyton from rocks, and a qual-

itative analysis of larval gut contents during this study revealed a dominance of diatoms and fine organic matter. Individuals have also been observed shredding leaves and feeding on the tissue of dead fish, although these modes of feeding are much less common than grazing. Case building behavior is typical of the Limnephiloidea (Ross 1967), wherein larvae enlarge the anterior end of the case with increasing instar age. As cases are enlarged anteriorly, that posterior portion of the case too narrow to accommodate the larval instar is typi- cally broken off. Early instars construct their cases out of leaves and twigs, but later switch to using small gravel exclusively, as has also been reported by Wiggins (1977). Additional life history features of D. giluipes have been reported by Lamberti and Resh (1979).

Methods S ~ u d y area

Research was conducted at the McCloud River (Shasta County, California), which is described in more detail by Tip- pets and Moyle (1978) and Wales (1939). The study site (eleva- tion of 640111) is located -7km downstream from McCloud Reservoir dam, which maintained a constant discharge (4.5 ms/s) during the study period. Mean daily water temperatures showed a small variation, increasing from -IVC at the outset of the study (31 May 1977) to -12OC at the study's completion (29 June 1977) (United States Geological Survey, unpublished data). There is a significant daily fluctuation in water temperatures, with a distinct early morning minimum that is 2-3°C lower than the late afternoon maximum.

Larval movements were studied in a single pool, approximately 35 m long by 15 m wide, which is bordered by steep, long riffles up- and down-stream. The pool's depth varies from 1 to 4 m, and the bottom consists of large stones and boulders (up to several metres in length) overlying smaller stones and gravel. Current speeds at various points across the pool bottom were always less than 20cm/s, and usually less than IOcmls. Periphyton (including diatoms, green algae, and detritus) occurs throughout the bottom, but no aquatic macrophytes are present. Underwater visibility during the study averaged 3-4m hori- zontally.

Collection, tagging, and release procedures In the middle of the pool, a 5 m x 10m area of relatively

uniform depth was marked off in I-mZ sections with small metal disks. Several collection sites on this 50-m2 grid were randomly selected, and 10-20 larvae were collected a t each of these locations. (Note: all underwater phases of this study were conducted while snorkeling or using SCUBA.) When available, a range of larval instars was purposely gathered at each site, taking care not to include moribund or molting individuals. The larvae to be marked were transferred to substrate-filled enamel pans placed underwater near the stream margin. The river current circulated freely over the pans, maintaining conditions comparable to those in which the larvae were collected. These seminatural conditions were designed to hold the larvae for several hours while individuals were being marked.

Plastic circular numbered tags (-2 mm in diameter, available from Chr. Graze KG, Postfach 2107, D-7056 Weinstadt-2, West Germany) wele attached to larval cases in two different ways.

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1176 CAN. J. ZOOL. VOL. 58, 1980

During the first study period (31 May - 6 June, 1977, hereafter called early June), a small piece of 0. I-mm diameter wire was looped through a hole placed in the tag. This wire loop tag was then twisted snugly around the case of each larva. In the second study (24-29 June, hereafter called late June), each numbered tag was attached to a rubber band (available from orthodontists) of slightly smaller diameter than the average larval case. This rubber band harness was then secured around the case (Fig. 1). Once a tag was in place, two measures of larval size were taken with a vernier micrometre caliper (accurate to 0.1 mm): the length of the case, and the lateral diameter of the anterior case opening. After a larva had been tagged and measured, it was immediately returned to its underwater pan. The time required for tagging and measuring averaged 2 min with the wire loop method, and -40s using the rubber harness. During this out- of-water tagging stage, larvae were dipped into water once or twice to keep their gills moist and reduce possible stress. Larvae from more than one pan were marked in a single "tagging ses- sion." After all the individuals in three to five pans were tagged, the larvae from each pan were released within 20 cm of the point of capture.

Mapping The x , y coordinates of each release point were noted on a

map attached to an underwater clipboard. Larval positions subsequent to release were recorded twice per day (-1200 and -2000 hours) for the next 6-7 days. During the search for larvae, each square metre quadrat was scannedfor astandard amount of time (15-30s). The map upon which locations were noted di- vided each square metre quadrat into twenty-five 20 cm x 20cm (400cm2) subquadrats, and a metre stick was used to determine the particular subquadrat in which each larva was located. Using this scale of spatial resolution, the minimum movement recorded for an individual was 20cm (i.e., if an individual moved from one subquadrat to an adjacent one), and larval movement within any given subquadrat was not recorded.

Since some of the released larvae moved beyond the 50-m2 gridded area, parts of the pool outside this grid were also sys-

FIG. 1. A tagged fourth instar D. gilvipes larva.

tematically searched. Because these areas were not gridded, searching for a uniform time period per unit area was difficult. In reality, searching effort was probably reduced outside the grid, lowering the probability of encountering a marked larva as it moved beyond the SO-m2 area. Nevertheless, a high percentage of larvae were relocated during both early and late June (see Results). The amount of time required to complete the underwater searching-mapping process averaged 1.5 h.

Sampling of behauior Tests to detect behavioral differences between marked and

unmarked larvae were based on data collected through focal- animal sampling (Altmann 1974). First, a complete list of behavioral states was made after observing numerous larvae over many hours. Focal individuals were chosen by generating a list of x, y grid coordinates from a random numbers table. After locating these coordinates within a quadrat, the two nearest marked and unmarked individuals were selected for observation.

The behavior of these randomly chosen larvae was quantified by recording each individual's behavioral state for sequential 5-s intervals. This record began and ended at predetermined times, usually lasting for 3.5 min per individual. Such a sample measures the manner whereby marked and unmarked larvae parti- tion their total time budget among various activities. These behavioral samples were always taken in the late afternoon.

Results Table 1 details the comparative time-activity

budgets of marked and unmarked larvae for the two studies. Six discrete behavioral states were identified, and are self-descriptive except for the following comments: (1) "feeding" was defined as those time intervals during which mandibular movement associated with grazing occurred; (2) when larvae crawling on steep rock faces slipped

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HART AND RESH 1177

TABLE 1. Results of the time-activity budget analyses, showing the mean percentage time (and standard error) spent by larvae

in the six different behavioral activities

Early June Late June

Behavioral Marked Unmarked Marked Unmarked category (n = 24) (n = 24) (n = 18) (n = 18)

Feeding on periphyton 70.4 74.9 80.0 86.4

(8.7) (8.2) (8.8) (7.5) Feeding on

leaves 0.3 0.0 0.0 0.0 (0.3)

Walking 8.4 3.6 1.8 2.4 (4.5) (2.6) (0.9) (0.9)

Withdrawn inside case 20.8 19.9 18.2 11.1

(8.5) (8.1) (9.0) (7.6) Holding onto

substrate 0.0 1.4 0.0 0.0 (1.4)

Falling 0.1 0.1 0 .0 0.1 (0.1) (0.1) (0.1)

NOTE: A Hotelling test indicated that no significant difference exists between the time-activ~ty budgets of marked and unmarked larvae during either study ( p > 0.40).

off, this was termed "falling." Greater than two- thirds of the total larval time-activity budget was spent feeding on periphyton in both studies.

To analyze these data statistically, the percent- ages were first converted to proportions, followed by an arcsin transformation to reduce nonnormality (Sokal and Rohlf 1969). A multiple analysis of vari- ance (ANOVA) was used to test the null hypothesis that the mean time spent in each of the six behavioral categories is the same for marked and unmarked larvae. No significant difference exists between the time-activity budgets of the two groups during either early or late June, when analyzed by Hotelling's F test ( p > 0.40). How- ever, there is some indication that both unmarked and marked larvae spend more time feeding in late June than in early June (0.05 < p < 0.10).

The collected field data describe the x, y locations of marked larvae at various times subsequent to release. Computer analysis of these data produced the following measures of distance and direction traveled by larvae (Fig. 2): (a) the Euclidean distance between an individual's present (xi, yi) and previous (xi-, , y,,) location; (b) the cumulative distance moved by an individual, summing the distances moved in each "step" from the point of release to its last recorded location; (c) the net, or straight-line distance between its last recorded location and the release point; (4 measures a , b, and

UPSTREAM n*

FIG. 2. Geometric representation of method by which successive x, y coordinates are used to generate measures of distance and direction, where DSTi = distance from point i to point i- 1;

cumulative DST = DST, = DST, + DST,; NETDST = i=, . .

distance betweenx,, y,andx,, y,;8 = direction of travel relative to upstream; O T = turn angle (= present direction of travel relative to previous bearing).

c were also calculated as the distance traveled di- vided by the time elapsed between observations, thus providing estimates of rates of movement; (e) the net direction (0"-360") moved by a larva from its point of release to its last recorded location, where 0" = directly upstream and 180" = directly downstream; and Cf) the direction turned by a larva, where three consecutive x, y coordinate pairs provide the minimum data required to calculate the "turn angle" formed by two consecutive "steps."

Table 2 summarizes the distances and rates of travel exhibited by marked larvae in early and late June. More than 100 larvae were tagged in each study, and in both instances a high percentage of these larvae were relocated one or more times after release. This high "relocation" value suggests that the bottom area searched was large enough to en- sure that most larvae confined their movement to within its borders. TABLE 2. Summary data indicating general distances and rates

of travel during the two study periods

Parameter Early June Late June

No. of larvae tagged 106 122

No." (and 91,) subsequently sighted 1 or more times 80(74.5) 96(78.7)

Mean cumulative distance traveled (and SE) (cm) 331 (27) 879 (71)

Maximum cumulative distance traveled (cm) 1047 3151

Mean distance traveled per hour (and SE) (cm/h) 5.5 (0.6) 14.4 (1.5)

Maximum distance traveled per hour (cm/h) 55.2 225.0

Mean net distance traveled (and SE) (cm) 229 (23) 547 (49)

Maximum net distance traveled (cm) 89 1 2502

This number also equals the sample size for each mean value determination listed below.

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1178 CAN. J. ZOOL. VOL. 58. 1980

Two broad conclusions can be drawn from the distance and rate data. First, larvae are neither sedentary nor do they show a strong homing tendency. If larvae characteristically returned to a given rock, as appears to be the case for some larval Trichoptera (Elliott 1970), one would expect that the net distance moved would approach zero. In both studies, however, the lower boundary of the 99% confidence interval for net distance lies well above 0, indicating that all larvae disperse some finite distance. Moreover, some individuals moved more than 25 m in only afew days. It is important to note here that the distance measurements obtained in this study are minimum estimates of the actual distances moved by individuals. This results from our use of the Euclidean formula which measures the straight line distance between two points, when in fact larvae seldom travel such a direct path. Second, larvae moved significantly farther (and at significantly faster rates) in late June (p < 0.01 for all comparisons), with rates of movement approximately 2-3 times greater than in early June.

The data were further analyzed by comparing the observed patterns of movement with random walk models, in order to determine whether larval movement is significantly nonrandom. In Brownian motion, the net distances traveled after a unit time by randomly diffusing molecules is described by a negative exponential distribution (Pielou 1977; Underwood 1977). This theoretical function is compared with the histogram describing the net distance moved per unit time for early June (Fig. 3) and late June (Fig. 4). In both cases, a x 2 analysis shows no significant difference between the observed and expected distributions (p > 0. I), indicating that the observed pattern of net distances traveled per unit time is well approximated by this random diffusion model.

Another component of any pattern of movement is the direction traveled by individuals. Histograms illustrating these directions of travel are shown for early June (Fig. 5) and late June (Fig. 6). There are at least two ways to analyze these directional patterns statistically. (1) A consideration of net dis- placement due to either upstream migration or downstream drift requires a comparison of the number of individuals moving upstream (270"-90") versus downstream (90"-270"). In neither study was there a significant difference between the number of larvae moving in these two directions ( p > 0.1, xZ test). (2) Alternatively, the histograms can be compared with the theoretical circular uniform distribution (Batschelet 1965), in which movements occur in all directions (0"-360") with equal Ere- quency. In early June, there is no significant differ-

ence between the observed and expected distributions (p > 0.25), whereas in late June a significant difference exists (p < 0.01). This latter deviation from randomness is caused by more larvae moving upstream or downstream than moving laterally. This movement pattern is not surprising, given that the shapes of the pool (15 m x 35 m) and the gridded zone (5 m x 10 m) are approximately twice as long as wide, thus constraining larval movement to predominantly follow the long (upstream-downstream) axis of the study site.

To explore this result further, a one-way ANOVA was used to determine whether the distance moved by a larva is independent of its direction of travel. The distances were transformed to logarithms in order to reduce the heterogeneity of variances (Sokal and Rohlf 1969). Cumulative and net distances, along with cumulative and net rates of travel, were compared between the following directional intervals: 3 15"-45" (upstream); 45"- 135" (lateral); 135"-225" (downstream); 225"-315" (lateral). For both early and late June, the results show that larvae moved significantly farther (and at faster rates) in the upstream and downstream directions relative to their movement laterally (p < 0.01). Note that the average net distance moved in the upstream and downstream direction is 1.8 (early June) and 1.9 (late June) times the distance moved laterally, corresponding well with the dimensions of the study site (length = 2 x width). However, a multiple comparisons test (Sokal and Rohlf 1969) showed no differences between distances (or rates) traveled when comparing upstream vs. downstream (p > 0. I), for either early or late June. This result indicates that if we stratify the directional alternatives so that spatial constraints are similar, larval movement is indeed independent of the direction traveled. Thus, all the above directional patterns agree with a random movement model, subject only to the obvious constraint of the rectan- gular habitat.

To determine whether a correlation exists in the successive directions traveled by larvae, the distribution of turn angles must be examined. Covariance per se cannot be readily calculated, but if no correlation is present between the directions of consecutive "steps," then a uniform distribution of turn angles results. Alternatively, larvae could tend to continue in the same approximate direction, as has been found for most studies of animal movement (see Pyke et al. 1977, and references therein). If so, the difference between the present and previous bearings would be minimal, thus pro- ducing a strong mode in the turn angle frequency distribution centered on O". (Note: for this analysis,

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HART AND RESH

EARLY JUNE LATE JUNE

NET DISTANCE MOVED (CWH) NET DISTANCE MOVED (CM/H)

DIRECTION OF TRAVEL DIRECTION OF TRAVEL

ANGLE TURNED RELATIVE TO PREVIOUS BEARING

ANGLE TURNED RELATIVE TO PREVIOUS BEARING

FIGS. 3-8. Figs. 3,4. Histogram of observed net rates of travel, along with the expected distribution produced by arandom diffusion model; the two distributions are not significantly different: early June ( x 2 = 7.8, df = 5, p > 0.10); late June k2 = 12.2, df = 8,p > 0.10). Fig. 5. Net directions of travel during early June; thisobserved distribution is not significantly different from a circular uniform distribution, in which movement occurs in all directions with equal frequency ( x2 = 13.3, df= 11,p > 0.25). Fig. 6. Net directions of travel during late June; this observed distribution is significantly different from a circular uniform distribution k2 = 34.0, df = l I , p < 0.01). Figs. 7, 8. Turn angle histogram for early and late June. If the direction traveled in one time interval (i.e., one "step") is independent of the direction traveled in the previous.time interval, aunifmm distribution would result. The observed distribution for early June is significantly nonuniform (XZ = 21.8, df = 11, p < 0.05); for late June, it is not significantly different from a uniform distribution (X2 = 10.6, df = 11,p > 0.25).

we redefine 0" as the turn angle an animal makes if it continues in a straight line from one "step" to the next.) The turn angle histograms are presented for early June (Fig. 7) and late June (Fig. 8). A X * test shows that the distribution is significantly nonrandom (i.e., nonuniform) for early June (p < 0.05), whereas the late June histogram does not significantly differ from uniformity (p > 0.25). Even in the nonrandom early June histogram, however, the distribution is not unimodal (p > 0.5, Rayleigh test; Batschelet 1965), in contrast to the above studies.

The random movement model also postulates that rates of movement should be independent of

the time of day. Because two mapping censuses were made per day, it is possible to compare "daytime" rates (i.e., rates of movement between - 1200 and -2000 hours on the same day) with "nighttime" rates (i.e., between -2000 and - 1200 hours on the following day). The mean "nighttime" versus "daytime" rates (and SE), in cen- timetres per hour, are 3.1 (0.4) vs. 11.4 (1.6), respectively, in early June, and4.8 (0.9) vs. 19.2(2.9), respectively, in late June. Thus, in both studies, larvae moved significantly farther per unit time (3-4 times faster) during the "daytime" (g < 0.01 for both dates).

To examine the relationship between the dis-

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1180 CAN. J . ZOOL. VOL. 58, 1980

tances traveled by larvae and larval body size, patterns of larval size must first be examined. Figure 9 presents a histogram of case widths for the two study periods. Although the use of case width as an index of body size is somewhat indirect, the data exhibit a clear pattern. The histogram shows a bimodal distribution in early June, and a unimodal distribution in late June. This agrees with head capsule measurements, indicating that both fourth and fifth instar larvae were present in early June, but that by late June all larvae had reached the fifth (final) instar. The mean larval case width in the first data set (i = 0.41 cm) is significantly smaller (p < 0.01) than the case width for the second data set (i = 0.52cm). Although this shift in body size could account for some of the increase in distances and rates of larval movement, changes in factors other than size which occurred simultaneously might confound such an interpretation. It is possible, however, to determine whether distances moved are independent of body size within each study period. Figures 10 and 11 illustrate this relationship for early and late June, respectively, demonstrating that body size and distance moved are positively correlated (p I 0.01 for both cases). This result suggests that body size is an important determinant of the distance moved by an individual. Neverthe- less, the low value of the coefficient of determination (R2 < 0.10 in both cases) indicates that much of the variation in movement is "explained" by factors in addition to body size.

Figure 12 provides an illustration of some typical patterns of movement by larvae. It serves to dem-

EARLY JUNE LATE JUNE

BODY SIZE INDEX BODY SIZE INDEX

FIGS. 10, 11. Scatter diagram and linear least-squares fit illustrating the correlation between a larva's rate of travel and its body size for early (Fig. 10) and late (Fig. 11) June. (Note: body size index = (case width)2 . (case length); rate of travel = (mean ~ m / h ) ' / ~ ) . A significant correlation exists between the two vari- ables: Spearman's coefficient of rank correlation. r , = +0.26, n = 80,p = 0.01 forearly June;r,= +0.29, n = 96,p< 0.005for late June.

01 I 0 1 2 3 4 5 6 7

DISTANCE (rn)

FIG. 12. Patterns of movement over the study interval by five typical larvae. Large dots indicate the point of origin of travel by the individual, small dots indicate the subsequent locations at -half-day intervals, and a "2" indicates that the individual remained at that locale for two successive periods.

19 .24 .29 .34 .39 44 .49 .54 .59 .64 .69

CASE WIDTH (cm) onstrate that the location of an individual through

FIG. 9. Histogram illustrating patterns of body size (as mea- time is highly patchy: i.e., larvae tend to remain in a

sured by case width) within the D. gilvipes population, with local area for several sampling intervals, and then open bars representing early June and shaded bars late June. move relatively large distances before again Mean (and SE) case width and length equal 0.41 (0.01) cm and "focusing" their activity in a circumscribed locale. 1.56 (0.04) cm for early June and 0.52 (0.006) cm and 2.03 (0.03) cm for late June. ~ h k distribution shows two distinct modes Discussion during early June when both fourth and fifth instar larvae were present; only one mode occurs in late June when only fifth instar Because the time-activity budgets of marked larvae were present. and unmarked larvae do not differ significantly, we

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HART AND RESH 1181

believe that the patterns of movement described here arc representative of unmarked R. gilripes in this habitat. These movement patterns are nl ways qualitatively (and usually quantitatively) similar to those predicted as the result of random processes. wilh three important exceptions, ui:. distances and rates of travel are not independent of larval size, time of day, or season. The significance of these exceptions is considered below.

In general, animal movement might be related to any of the following ecological processes: (a) selection of optimal microhabitats along abiotic environmental gradients; (b) colonization of unsatu- rated habitats, as has been suggested for invertebrate drift (Miiller 1954) and upstream migration (Williams and Hynes 1976); ( r ) habitat shifts associated with life history changes, as with pupation site selection occurring near the completion of the larval stage (Hultin cr 01. 1469; Otto 197 1): (4 behavioral interactions with conspesifics, including in tetference competition (McLay 1968; Glass and Bovbjerg 1969) and mate-related reproductive activities (Solem 1976); (e) predator avoidance, either spatially (Charnov er ol. 1976. p. 249. Fig. I) or temporally (Allan 1978): If) foraging behavior. especial1 y where food is patchy in distribution and limiting in abundance (Townsend and Hildrew 1976). By considering the ecology of D. giluipes in detail, it is possible to evaluate the relative importance of those environmental factors likely to influence its patterns of movement.

The pool habitat studied here showed no pro- nounced environmental gradients in physical features (cf. (a) above). Turbulence prevented the development of stratification in either temperature or oxygen concentration. Current speeds were uni- formly low in the pool, and larvae showed no rheohxis (cf. Boumaud 1974) under these conditions. Likewise. D. gilrlipes displayed no marked substrate size selection. We conclude that abiotic heterogeneity is unlikely to be a prime factor influencing these movement patterns.

Migration-related upstream movements (cf. (b ) above) by larvae can he ruled out for two reasons: 113 the directianality data show no significant difference between the distances moved in these two directions; and (2) adult D. gil~ipcs are large. strong fliers which can easily ff y upstream. whereas larvae do not move against the swift currents present in the river's steep riffles.

Although prepupat Eon movements (cf. (c) above) have been documented in other caddis larvae (e,g., Orto 197 I). and also occur in D, gilcipes, it is unlikely that the movements observed here were pupation related, First, the prepupal resting stage did

not occur until August, some 1-2 months after the data described here were collected. Second, pupation occurs in the same pool in which the larvae were studied, meaning that alarva traveling at typical speeds could reach any "preferred" pupation site within 2-3 days. Hence, there is no obvious reason why larvae should be moving toward pupation sites on such an accelerated schedule.

During the larval stage of D. gilvipes, no intra- specific behavioral interactions (cf. (d) above) were observed. Field and laboratory observations indicate that the response of these larvae to con- specifics is largely indistinguishable from their behavior towards abiotic components of the environment. In addition, movements related to mating activities take place only during the adult stage of the life cycle (in September and October).

There are several reasons for believing that the movements of D. gilvipes are unrelated to predator avoidance (cf. (e) above). First, in over lOOh of underwater observation, the major predators present in the pool (satmonids) were frequently seen feeding on drifting insects, while epibenthic feeding was never observed. Although D. gilt ' I p e.7 was a large, active, and dense prey item (,scns14 Ware 1973), the fish did not select them. Even when larvae were experimentally placed in the "drift," fish would capture only those individuals which had been removed from their cases. Stoneffy nymphs similarly placed in the drift were readily captured. Second. if predation were a significant source of larval mortality. one might expect strong selection in favor of reduced activity during periods of peak predation (e.g,, Thorne 1969; Allan 1978). Visually feeding salmonids are most capable of detecting prey during daylight hours. and yet this is precisely the t ime when larvae are most mobile (cf. Results). Although the adaptive significance of this die1 rhythm in activity is still uncertain (but see below), these observed larval movement patterns do not seem to be related to vertebrate predation in any obvious way. These observations are in distinct contrast to the results of Tippets and Moyle (1978), which suggest that rainbow trout in the McCloud River feed largely on epibenthos rather than drift. However, our study took place when turbidity in the river was lower than that reported by Tippets and Moyle, perhaps causing a shift in the foraging behavior of the trout.

Having suggested that these movement patterns are not prominently influenced by any of the pre- ceding factors, the relative importance of movement as a foraging behavior can now be evaluated. There is little doubt that foraging is a major component of the larval ecology of this species. As a rule,

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1182 CAN. J. ZOOL. VOL. 58, 1980

the immature stage in aquatic insect life cycles functions as an energy gatherer, whereas the adult stage serves primarily for reproduction and dispersal (Hynes 1970). Furthermore, greater than two- thirds of the average larval time budget was spent feeding (Table 1).

If preferred food types were homogeneously distributed and nonlimiting, there would be no reason to expect that larval movements should be related to foraging. However, there are several indi- cations that food resources are patchy, and scarce relative to demand. Although we did not quantitatively analyze the distribution and abundance of the periphyton upon which these larvae fed, gross differences in periphyton "thickness" and percentage cover could be detected visually (cf. Stimson 1970). In fact, some workers have used this visually-based method to quantify periphyton standing crops (e.g., Blum 1957; Haven 1973). Standing crop of periphyton was observed to vary greatly over the 15 m x 35 m study area. Patchiness was observed on several spatial scales: e.g., small-scale discon- tinuities in periphyton abundance were visible at the centimetre-to-centimetre level of resolution, whereas large-scale heterogeneity was illustrated by entire sections of the stream bottom (1 m2 or larger) containing very little periphyton, relative to other zones in which such food was abundant (cf. Jones 1974; Bowen 1978; and Tett et al. 1978; where periphyton spatial heterogeneity has been quantified). In relation to these scales and degrees of patchiness, the mapped location patterns (Fig. 12) suggest that the individual larvae often remain in one general area for several days, and then move well away from their previous position before again becoming less mobile. The small-scale grazing patterns of larvae show that they do not feed con- tinuously while moving, but instead move relatively large distances between consecutive locales at which intensive grazing occurs. One of us (Hart .

1980) has demonstrated that these small-scale movement patterns are strikingly influenced by spatial heterogeneity in the availability of periphyton. In particular, the rate of movement across small-scale food patches is negatively correlated with the amount of periphyton present per patch.

Not only do larvae behave as though food patchiness were present, there are strong indica- tions that food is actually limiting in abundance. Larvae are able to deplete periphyton standing crops, as evidenced by the great increase in periphyton biomass on colonization plates in which D. gilvipes were excluded, relative to controls on which larvae could freely graze (D. D. Hart, unpublished data). In addition, shortly after larvae

began their prepupal resting stage and ceased grazing, periphyton standing crops on the river bottom increased markedly. By itself, however, this information does not indicate whether the degree of food depletion effected by larvae produces conditions of actual food limitation.

Thus, it becomes essential to consider the relationship between body size and distances (or rates) traveled by larvae. Recall that in both early and late June, large individuals moved significantly farther (and at significantly faster rates) than small individuals. How can this result be interpreted? Within a species, large insects have greater metabolic requirements (e.g.. calories ex- pended per individual per day) than small insects (Keister and Buck 1964). If food density was low, and similar for all individuals, larger individuals would have to move farther than smaller ones since their food needs could only be met by foraging in a larger area. Vertebrate ecologists have noted similar interspecific patterns in the relationship between body size, metabolic rate, and home range size (e.g., McNab 1963; Schoener 1968, 1971; Turner et al. 1969). We suggest that the distance moved by a larva is correlated to its body size because food is locally limiting, requiring that larger individuals move farther to meet their greater metabolic requirements. Other work on stream insects complements this conclusion, in that mobility increases when food availability is experimentally reduced (Elliott 1970; Hildebrand 1974; Ketler 1475; Gallepp 1977). The study of Hazlett and Rittschof (1975) agrees with this line of reasoning. They argue that the lack of correlation between distance moved and body size in spider crabs is an indication that resources are not locally limiting.

The diel rhythm in locomotory activity may also be related to foraging. Little is known about the sensory receptors that Trichoptera larvae use while foraging. although many studies indicate that the simple eyes (i-e.. sternrnata) of larval insects aid in orientation (cf. Wigglesworth 1973). If visual stimuli are invdved. foraging should be easier during daylight. Alternatively, this diel pattern may be connected to the fact that both ingestion rates and assimilation efficiencies are often positively correlated with temperature (e.g., Otto 1974; Heiman and Knight 1975; Zimmerman and Wissing 1978). Bemuse of the daily temperature pattern of early morning minima and late afternoon maxima. energy gain per unit time may be greater during the "daytime" interval studied here, thus providing a selective premium for maximized foraging rates at these times. Nevertheless, observations made at night show that at least some larvae also feed during

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HART AND RESH 1183

that time interval. Whether or not these hypotheses are correct. however. this diel pattern cannot be due to a simple &-type effect of temperature on locomotory activity (cf. Shapley 1924: Keister and Buck 1964): the daily temperature range is 2-3°C. whereas movement rates differed by a factor of 3-4. In addition. a similar diel pattern of activity has been noted for D. g i l ~ i p m in the lab. where temperatures varied less than 1°C on a daily basis.

Perhaps the most striking result of this study is the substantial difference in distances and rates of movement between early and late June. Larvae traveled -3 times farlher (and faster) after a period of only 20-25 days. The temperature increase that occurred over this time interval was quite small (-2°C. United States Geological Survey. unpublished data), and insufficient to explain the increased movement as a simple response of locomotion to temperature (see above references). We believe the key to understanding this relationship between movement patterns and time of year lies in the phenology of larval food requirements.

Food requirements change during larval development in many insects. The amount of food ingested per individual increases sharply with older instars, and many insects consume far more than 50% of their total larval food intake during the last instar alone (Waldbauer 1968). Winterbourn (197 1) and Anderson and Grafius (1975) have shown that caddis larvae require much greater amounts of food per individual in the final instar, and Otto (1971), Winterbourn (1971), and Anderson and Cummins (1979) have suggested that larvae require a par- ticularly rich food supply in this period prior to pupation. A large weight loss occurs during pupation (Winterbourn 1971; Resh 1977), and this loss must be even more extreme in species like D. gilvipes which also have a prepupal resting stage. Thus, final instar caddis larvae are probably adapted to store energy and other nutrients for the subsequent nonfeeding pupal and adult stages. On average. since larger larvae produce larger adults. and fecundity is positively correlated with adult body weight (e-g.. Southwood 1979; Clifford and Boerger 1974), high food intake during the last instar translates into increased Darwinian fitness in a manner that makes large weight gains clearly adaptive.

Certain field observations made thus far seem to fit the above generalized patterns. For example, D. gilvipes larvae appear to devote more time to feeding in late June (fifth instar only) than in early June (fourth and fifth instars). Qualitative patterns of electivity (sensu Ivlev 1961) also change during larval development. Food types on the river bottom

other than periphyton are rare during the spring and summer. However, maturing Acer circinatum leaves are occasionally blown off a tree and into the river. (Note: these undecayed, green leaves should not be confused with the senescent or dead leaves common during autumn leaf-fall.) The degree to which larvae select such rare food items showed an unexpected pattern, in that fourth instar larvae fed upon but showed no marked preference for Acer leaves that they encountered. Late final instar larvae, on the other hand, showed a marked preference for similarly unconditioned Acer leaves, and the density of grazing larvae on such rare food types was 5-10 times greater than densities on adjacent periphyton. Such observations are not acci- dental, as this preference by final instar larvae for rare food items has been observed many times, and in several streams (Hart 1980). Because these leaves are composed of less ash than the diatom- dominated periphyton (cf. Cumrnins and Wuycheck 1971), this change in electivity is con- sistent with the hypothesis that food quality is an increasingly important aspect of food selection prior to the prepupal resting stage. Thus, the increased movement of fifth relative to fourth instar larvae may be due to at least two interacting factors: (1) final instar larvae consume greater amounts of food, and must forage greater distances to meet these requirements, since food is locally limiting; (2) greater mobility could increase the probability that final instar larvae would encounter "rare but preferred" food items, at a time when food quality and energy storage are of critical importance.

Acknowledgments Many individuals assisted in this research, but

we especially thank S. Hart, T. Coon, E. McEl- ravy, G. Lamberti, and the Diving Control Board of the University of California, Davis. Drs. P. Moyle, P. Richerson, D. Wilson. and two anonymous re- viewers read the manuscript and provided many helpful suggestions. The research leading to this publication was supported by National Science Foundation dissertation grant DEB 77-20800, a Chancellor's Graduate Research Award, and a University Graduate Fellowship (to D.D.H.); the Nature Conservancy, Office of Water Research and Technology, United States Department of the Interior. under the allotment program of Public Law 88-379. as amended. and the University of California Water Resources Center. as part of Office of Water Research and Technology project No. A-063-CAL and Water Resources Center project UCAL-WRC-W-5 19 (to V.H.R.).

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movement patterns and foraging ecology of a stream caddisfly larva

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