Intraguild predation and cannibalism among larvae of detritovorous caddisflies in subalpine wetlands.
Although it has long been documented that potential competitors also prey on each other (e.g., Paine 1963), it is only recently that the taxonomic and ecological ubiquity of intraguild predation (IGP) has been appreciated by ecologists (see reviews by Ebenman and Persson 1988, Polis et al. 1989, Polis and Holt 1992). Cannibalism, which can be considered the special case in which intraspecific competitors eat each other, is often reported within populations of species that interact as intraguild predators (Fox 1975, Polis 1981, 1988, Elgar and Crespi 1992). Both interactions are common in guilds of omnivorous (sensu Pimm 1978) predators in which larger species (or conspecifics) prey on smaller species or individuals within a species (reviewed by Polis et al. 1989; also see Hurd and Eisenberg 1990, Spiller and Schoener 1990, Wissinger and McGrady 1993). Intraguild predation is also common among similarly sized species that exhibit dramatic size increases during ontogeny (fish, amphibians, long-lived invertebrates such as lobster, scorpions; Werner and Gilliam 1984, Wilbur 1984, 1988, Ebenman and Persson 1988, Polis et al. 1989). Even in short-lived invertebrate predators (e.g., many aquatic and terrestrial insects), phenological differences between species and/or asynchronous development within generations can lead to temporal overlap of different size classes of conspecifics and heterospecifics, and hence to IGP and cannibalism (Hurd 1988, Wissinger 1989, 1992). Despite increased appreciation for the widespread occurrence of IGP and cannibalism, the community level ramifications of these interactions are understood for only a few well-studied systems (Polis and Holt 1992).
The stimulus for the experiments described in this paper was the observation that two morphologically and ecologically similar limnephilid caddisflies reciprocally dominate in subalpine wetlands that differ mainly in degree of permanence. The two species have nearly identical life cycles and both can exploit temporary waters because adults lay eggs terrestrially at the edge of pond basins (see Caddisfly Natural History, in the next section). However, in the wetland complex at our study site, Asynarchus nigriculus Banks is always dominant in temporary and Limnephilus externus (Hagen) is dominant in permanent basins (S. A. Wissinger and W. S. Brown, unpublished manuscript; [ILLUSTRATION FOR FIGURE 1 OMITTED]). This pattern is even more striking in single, isolated ponds near our study site where L. externus and A. nigriculus are completely segregated in permanent and temporary waters, respectively (S. A. Wissinger and W. S. Brown, unpublished manuscript). Previous workers at this site have studied the mechanisms that underlie inter-basin differences in zooplankton species composition (Dodson 1970, 1974, Sprules 1972), but little is known about the factors that are responsible for the dramatic inter-basin differences in the benthic communities (S. A. Wissinger, unpublished manuscript).
In this paper we present experimental evidence that intraguild predation and cannibalism occur among larvae of Limnephilus and Asynarchus and suggest that asymmetric IGP plays a major role in determining patterns of distribution and abundance of these species. We initially assumed that these limnephilid caddisflies were mainly shredders of vascular plant detritus (Wiggins 1973, 1977, Barlocher et al. 1978, Williams and Williams 1980, Berte and Pritchard 1986). Thus, the first experiment was designed to test the hypothesis that habitat-specific differences in the outcome of intra- and/or interspecific competition were responsible for observed patterns of distribution and abundance (as in Park 1954; other examples reviewed by Dunson and Travis 1991, Warner et al. 1993). We report that (1) there is little evidence for resource competition per se between these species; (2) IGP and cannibalism are the main interactions that occur among their larvae; and (3) in the absence of other biotic interactions, the outcome of interactions between these two species should be the same in both permanent and temporary habitats. We also provide evidence that behavioral differences in aggressiveness and phenological differences in the timing of development are mechanisms that underlie the asymmetry in IGP between these species. Finally, we discuss the advantages of IGP and cannibalism for detritivores in the context of the low nutrient quality of detritus in these high elevation, oligotrophic waters.
STUDY SITE AND CADDISFLY NATURAL HISTORY
The study was conducted in the Elk Mountains of central Colorado at the Mexican Cut Nature Preserve, a pristine, subalpine (3640 m elevation) wilderness area owned by The Nature Conservancy and managed by the Rocky Mountain Biological Laboratory. The preserve contains several wetland complexes with [greater than] 50 shallow basins that vary in area (5-4650 [m.sup.2]), water chemistry, hydroperiod, and community composition (Dodson 1970, 1974, 1982, Maly 1970, 1973, Sprules 1972, Wissinger and Whiteman 1992). Basins are either permanent, temporary autumnal (sometimes dry in autumn), or temporary vernal (always dry in early summer; after Ward 1992) depending on their size, morphometry, and exposure (see additional details in Wissinger and Whiteman 1992). Hydroperiod is the most predictive abiotic correlate of distributional patterns among the 15 plank-tonic and [greater than] 70 benthic invertebrates that occur in the wetland complex (S. A. Wissinger, unpublished manuscript). The only aquatic vertebrate in the system is the tiger salamander, Ambystoma tigrinum nebulosum (Hallowell), which breeds in the permanent and some autumnal basins on the preserve (Whiteman et al. 1994). Only permanent habitats contain the life stages ([greater than] 1-yr-old larvae and paedomorphs) that prey on benthic invertebrates (Whiteman et al. 1994, 1996).
Asynarchus nigriculus and Limnephilus externus are among the most abundant and conspicuous macroinvertebrates at Mexican Cut. Dietary analyses revealed that the two species have nearly identical diets, with vascular plant detritus and benthic algae comprising [approximately equal to]95% of gut contents by volume (Sparks 1993). Limnephilus larvae build haphazardly constructed cases from fragments of aquatic plants (mainly Isoetes bolanderi), whereas Asynarchus build exquisite patchwork tubes from fragments of spruce bark, spruce needles, and bits of stone. Despite differences in case structure, the two species are nearly identical in body size at each of the five larval instars, and have generally similar life histories that differ slightly in phenology. Adults of both species lay eggs under rocks and logs along the shoreline of basins. Eggs overwinter under 10-15 m of snow and hatch in spring when all basins are full. Asynarchus hatch earlier and develop faster than Limnephilus so that at a given time within basins, Asynarchus are typically one to two larval instars ahead of Limnephilus (S. A. Wissinger and W. S. Brown, unpublished manuscript). This developmental head start allows Asynarchus, but not Limnephilus, to exploit rock pools and other vernal basins that dry early in summer [ILLUSTRATION FOR FIGURE 1 OMITTED]. However, both species complete larval development, pupate, and emerge before autumnal basins dry (S. A. Wissinger and W. S. Brown, unpublished manuscript). Thus, the pattern of reciprocal dominance between autumnal and permanent habitats is not the result of life cycle/history constraints [ILLUSTRATION FOR FIGURE 1 OMITTED].
Competition field experiment
The first experiment was conducted in July 1992 and was designed to (1) quantify the relative strengths of intra- and interspecific competition among larvae of the two caddisflies and (2) determine if the outcome of competition varied between permanent and autumnal habitats. Six screened (1-mm mesh) wood frame cages (0.5 m cubes; 0.25 [m.sup.2] bottom area) were placed in the littoral zone of four permanent and four autumnal basins. Both species were abundant in these eight habitats, and natural densities in open areas near the cages were similar to those in the cages during the experiment. After the cage bottoms were sealed with clay, salamanders, caddisflies, and large invertebrate predators (e.g., Dytsiscus beetle larvae) were removed. We re-checked the cages several times for caddisfly immigration before the experimental organisms were introduced.
The following treatments were randomly assigned to the cages in each pond: (1) Asynarchus at low density, (2) Asynarchus at high density, (3) Limnephilus at low density, (4) Limnephilus at high density, (5) both species at high density, and (6) cage control for immigration (no caddisflies). The cage controls revealed that the cages were effective in excluding immigrants during the duration of this and subsequent experiments. Low and high (single and mixed) density treatments of 200 and 400 larvae/[m.sup.2], respectively, bracket combined densities of shoreline populations of the two species in these habitats. The larval instars used for each species were representative of those present in the natural populations at the time of experimental set-up (9:1 - fifth (final): fourth instar Asynarchus, and 3:2 second: third instar Limnephilus). Twenty larvae of each species at these instar ratios were sampled from the pool of larvae used for the experiment to estimate the initial masses of each instar. These larvae were killed in 90% ethanol and immediately dried at 50 [degrees] C for 24 h and the mass determined to the nearest microgram on a Cahn C31 electrobalance (Cahn, Incorporated, Cerritos, California). All values for mass reported in this paper were determined in this way.
Larval development proceeded rapidly during the experiment, which was terminated after 10 d when Asynarchus began to pupate. All surviving animals were removed, sorted into instar classes, and counted. Pupae and larvae from each experimental unit were killed in 90% ethanol, and all pupae and 20 larvae were dried and the mass determined to the nearest microgram.
The experiment was analyzed as a split-plot design with four ponds nested in each hydroperiod type (i.e., n = 4), and treatments replicated over all basins (i.e., n = 8). We initially analyzed the growth and survival of larvae simultaneously using MANOVA and found that the dependent variables were not correlated (Bartlett's tests of sphericity all [much greater than]0.05; see Norusis 1990). Thus, the analyses presented here are based on split-plot ANOVA for the effects of hydroperiod and treatment on the growth and survival of each species. In this and subsequent ANOVA models, significant differences among means were based on Scheffe's method for unplanned a posteriori contrasts (see Day and Quinn 1989). Proportional survivorship data were arcsine-transformed to approximate assumptions of normality. Bartlett-Box and Lilliefors statistics in this and subsequent analyses were used to test for assumptions of homoscedasticity and normality, respectively (Norusis 1990).
Laboratory behavioral studies
The results of the competition field experiment prompted several behavioral studies that were conducted in July through August 1992 in a portable field laboratory at the site. We observed caddisfly behaviors in plastic storage containers (0.25 [m.sup.2] bottom area) that contained [approximately equal to]2.5 cm of detritus, a clump of emergent vegetation, three small rocks, and several pieces of woody debris. Twelve arenas were filled with pond water to a depth of [approximately equal to] 10 cm and then assigned one of the following treatments: (1) fifth-instar Asynarchus alone, (2) fourth-instar Limnephilus alone, and (3) both species. Densities in all arenas were maintained at 200 larvae/[m.sup.2], which corresponded to the low density treatments in the competition field experiment. Two observational protocols were used in the arenas. First, we conducted 10 min focal animal samples and recorded activity levels (time spent crawling, distance crawled, and time spent foraging), and behaviors associated with aggression (proleg wrestling, case shaking, and biting). Secondly, we recorded all encounters observed during 10 min of scanning an arena and noted whether the encounter was aggressive and which species was the aggressor. Three observers worked simultaneously with one of the three treatments; thus, time of day and between-day effects should not bias comparisons among treatments. Observations were made between 0900 and 1600.
Because of the multiple dependent variables (time spent foraging, time spent crawling, and distance crawled), we analyzed the data from focal animal observations using a two-way MANOVA (species x treatment). The proportion of encounters that resulted in aggression was analyzed using a two-way ANOVA (species x treatment) on arcsine-transformed data.
Size-dependent intraguild predation
The results of the competition field experiment and the laboratory experiments prompted a second field experiment designed to determine whether Asynarchus predation on Limnephilus was facilitated by a size advantage that results from a phenologic head start. In July 1993, we placed 16 enclosures (same as in the competition experiment) in the littoral zone of one of the permanent basins (Wissinger and Whiteman 1992: pond L1). The following treatments were randomly assigned to the enclosures: (1) same-sized Limnephilus and Asynarchus (all fifth instars), (2) large Asynarchus (fifth instars) with small Limnephilus (third instars), (3) small Asynarchus (third instars) with large Limnephilus (fifth instars), and (4) a no-caddisfly cage control to monitor cage permeability. Densities were the same as those used in the mixed species treatments in the first field experiment (200 + 200 = 400 larvae/[m.sup.2]). Large Asynarchus and small Limnephilus were obtained from the Mexican Cut ponds where they naturally coexist. We exploited intraspecific differences in phenology across elevations to obtain the other size combinations. Small Asynarchus were taken from several ponds near Mexican Cut that occur at a higher elevation (3700 m) than the experimental ponds, and large Limnephilus were obtained from ponds at lower elevations (3100 m) near the Rocky Mountain Biological Laboratory.
The experiment was terminated after 10 d, when all surviving larvae and pupae were removed from the cages and counted. We initially analyzed the number of each species surviving with a one-way MANOVA and found no correlation between Limnephilus and Asynarchus survival. We subsequently conducted a one-way ANOVA on each species.
Density-dependent Asynarchus cannibalism
Results of the competition experiment, laboratory studies, and field observations all suggested that cannibalism is a commonplace interaction among Asynarchus larvae. To determine if cannibalism is density-dependent, we conducted a third field experiment in one of the autumnal basins that supports especially high densities of Asynarchus (Wissinger and Whiteman 1992: pond L8). Peak densities for final instar Asynarchus in that pond were 300-400 larvael[m.sup.2] (S. Wissinger and J. Jannot, unpublished data). Because we were interested in determining whether cannibalism would occur at lower than ambient densities, we stocked the field enclosures with 100, 200, and 400 Asynarchus larvael[m.sup.2]. Each of the density treatments and an empty cage control were replicated three times with the treatments randomly assigned to the 12 enclosures. We initiated the experiment in early July using 1:2:1 ratios of second: third: fourth instars of Asynarchus, which reflected the natural ratios in that pond at the time of experimental set-up. Ten individuals of each of these instars were collected at the start of the experiment and weighed to the nearest microgram. The experiment was conducted for 14 d, after which all larvae and pupae were removed and counted. Twenty animals from each experimental unit were kept to determine final mass. We analyzed the effect of density on larval mass and survival with one-way MANOVA and on the proportion that pupated with one-way ANOVA on arcsine-transformed data.
Competition field experiment
Growth. - Both species grew rapidly in permanent and autumnal habitats [ILLUSTRATION FOR FIGURE 2 OMITTED]. By the end of the experiment, all Asynarchus were in the final instar or had begun to pupate. Final average masses of Limnephilus and Asynarchus larvae were consistently greater in permanent than in autumnal habitats, although this hydroperiod effect was not statistically significant (Table 1, [ILLUSTRATION FOR FIGURE 2 OMITTED]). Neither an increase in intra- nor interspecific densities resulted in a change in growth rates for either species (Table 1, [ILLUSTRATION FOR FIGURE 2 OMITTED]). However, there was a treatment effect on the final mass of Asynarchus pupae (split-plot ANOVA; treatment effect [F.sub.2,12] = 15.2, P = 0.001). Asynarchus pupae in the mixed species treatments had significantly more mass than those in either the low or high single-species treatment (Scheffe's a posteriori contrast, P = 0.001 and P [less than] 0.001, respectively). Hydroperiod did not affect pupal mass (split-plot ANOVA; hydroperiod effect [F.sub.1,6] = 1.4, P = 0.28).
Survival. - Neither Asynarchus nor Limnephilus survival was affected by hydroperiod, and Asynarchus survival did not differ among treatments (Table 1, [ILLUSTRATION FOR FIGURE 3 OMITTED]). However, Limnephilus survival was much lower in the presence of Asynarchus than in either of the single-species treatments (Table 1, [ILLUSTRATION FOR FIGURE 3 OMITTED]). Over 80% of the Limnephilus survived in the high and low single-species treatments, but only [approximately equal to]20% survived in the presence of Asynarchus. Across all ponds, Limnephilus survival in single-species treatments (low density, 0.84 [+ or -] 0.11; high density 0.87 [+ or -] 0.15; mean [+ or -] 1 SE) was higher than that of Asynarchus (low density, 0.75 [+ or -] 0.07; high density, 0.67 [+ or -] 0.05; ANOVA, [F.sub.3,26] = 3.55, P = 0.03).
Laboratory behavioral studies
Asynarchus was more active than Limnephilus in the observation arenas, and was clearly the more aggressive of the two species. Head-to-head Asynarchus encounters with Limnephilus and conspecifics often involved proleg wrestling and biting, and occasionally escalated into intraguild predation or cannibalism. Asynarchus larvae also "attacked" and vigorously shook the posterior end of the cases of other larvae. Limnephilus often responded to aggressive encounters by retreating into their cases. The presence of heterospecific larvae did not affect the level of aggressiveness for either species (two-way ANOVA main effects of treatment: Asynarchus [F.sub.1,18] = 0.635, P = 0.55; Limnephilus [F.sub.1,14] = 0.335, P = 0.60). Across all treatments, [greater than]30% of the encounters initiated by Asynarchus resulted in aggressive behavior, compared to only 7% for Limnephilus ([F.sub.1,20] = 6.87, P = 0.01; [ILLUSTRATION FOR FIGURE 4 OMITTED]). The predation events we observed during focal animal samples, during encounter samples, between samples, and in holding containers always involved Asynarchus as the predator, either on Limnephilus or on a conspecific. Asynarchus predation on Limnephilus usually occurred between one predator and one prey, whereas Asynarchus cannibalism typically involved several predators mobbing a single conspecific. After conspecific victims were consumed, the aggressors dismantled the case and added the fragments to their own cases before dispersing. Limnephilus cases were not dismantled after Asynarchus IGP.
Size-dependent intraguild predation
In this field experiment, we manipulated the relative size of the two caddisfly species and found that Asynarchus survival did not differ among treatments (univariate [F.sub.2,9] = 2.34, P = 0.16). However, Limnephilus survival did differ among treatments ([F.sub.2,9] = 67.2, P [less than] 0.001; [ILLUSTRATION FOR FIGURE 5 OMITTED]). Fewer Limnephilus survived in the presence of large Asynarchus than in treatments in which the two species were similar in size, and in treatments in which large Limnephilus were with small Asynarchus (Scheffe's a posteriori contrast, P [less than] 0.001). There was no evidence that large Limnephilus prey on small Asynarchus, and Limnephilus and Asynarchus survival rates varied independently across treatments (Bartlett Test of Sphericity = 1.37, P = 0.24).
Density-dependent Asynarchus cannibalism
In the cannibalism field experiment, Asynarchus survival was relatively low ([approximately equal]40%) in all treatments as compared to in the competition field experiment. The average mass of survivors was not correlated with the proportion of larvae that survived (MANOVA Bartlett Test of Sphericity = 1.04, P = 0.35). Asynarchus survival did not differ across the different treatment densities ([ILLUSTRATION FOR FIGURE 6 OMITTED]; MANOVA univariate F test for survival [F.sub.2,9] = 0.265, P = 0.77), but density did affect the final mass of larvae (MANOVA univariate [F.sub.2,9] = 7.53, P = 0.012; [ILLUSTRATION FOR FIGURE 7 OMITTED]). At the end of the experiment, average final mass of larvae at the highest density (400 larvae/[m.sup.2]) was lower than at the other two densities (Scheffe's a posteriori contrast, P [less than] 0.05).
Asymmetric Asynarchus IGP on Limnephilus
Our results suggest that Asynarchus and Limnephilus interact mainly as intraguild predator and prey, respectively. Although the two species have nearly identical diets and exploit similar microhabitats, it does not appear that exploitative intra- or interspecific competition is an important interaction, at least at the densities at which larvae naturally occur at and near our study site. By manipulating the relative sizes of these two species, we found that Asynarchus IGP on Limnephilus is facilitated by a developmental size advantage that Asynarchus enjoys as a result of earlier hatching in spring. Phenological priority appears to be extremely important in creating the potential for asymmetric IGP [TABULAR DATA FOR TABLE 1 OMITTED] interactions among aquatic predators (Benke 1978, Morin 1984, Wilbur and Alford 1985, Wissinger 1989). As has been noted for amphibians (e.g., Wilbur and Alford 1985), early and rapid development in caddisflies both facilitates the exploitation of ephemeral habitats and confers a competitive and/or predatory advantage over other species.
Asymmetry in IGP between these two species is also related to differences in aggressiveness. In the second field experiment, we observed that Limnephilus did not prey on Asynarchus even when they had a size advantage. This result is not surprising given the differences in aggressive behavior that we observed in the laboratory experiments. In the laboratory arenas, we observed that Asynarchus frequently disrupt Limnephilus foraging by forcing them to retreat into their cases upon attack. Thus, in addition to the mortality effect, Asynarchus should have sublethal effects on Limnephilus fitness (as in Skelly and Wemer 1990; Peckarsky and Cowan 1991; Peckarsky et al. 1993 and references therein). Such sublethal effects would have been difficult to detect in the field experiment because Asynarchus IGP greatly reduced the densities of Limnephilus and was probably selective on the smallest Limnephilus.
Our results suggest that the dominance of Asynarchus in autumnal habitats at Mexican Cut is a result of asymmetric IGP, but they do not explain the dominance of Limnephilus in permanent ponds. Both species grew slightly faster in permanent than in temporary habitats, and survival did not differ among habitats for either species. Thus, in the absence of other biotic interactions, Asynarchus should dominate in all habitats. Elsewhere, we show that the dominance of Limnephilus in permanent habitats is in part an indirect positive effect of salamander predation on Asynarchus (S. A. Wissinger, G. L. Rouse, G. B. Sparks, W. S. Brown, and H. H. Whiteman, unpublished manuscript).
Asynarchus predation on Limnephilus is usually a one-on-one phenomenon, whereas Asynarchus cannibalism usually involves a mob of attacking conspecifics. The phenomenon is easily observed in the field at our study site because of the clear, shallow waters; the number (3-10) of animals that coalesce to devour the victim; and the frenetic behavior of the attackers. We do not as yet understand the cues by which these mobs form or the characteristics of victims that make them vulnerable. Preliminary experiments suggest that animals that have recently molted might be especially vulnerable (S. A. Wissinger, personal observation). To our knowledge, group cannibalism has not been previously described in limnephilid caddisflies or in any aquatic insect.
Asynarchus cannibalism also differs from predation on Limnephilus in that it frequently occurs among larvae that are of similar size. Non-filial cannibalism in many, if not most species for which it has been described, usually involves larger animals preying on smaller conspecifics (see reviews by Fox 1975, Polis 1981, 1988). In contrast, Asynarchus development is univoltine and relatively synchronous so that most animals are the same size at the same time, and a priori, the opportunity for cannibalism might be predicted to be relatively low (Wissinger 1992). That attackers and victims are the same size may explain why we rarely observed one-on-one cannibalism events between Asynarchus.
Asynarchus cannibalism is apparently not an extraordinary event related to crowded conditions or starvation. We observed similar rates of cannibalism at lower than ambient densities in the cannibalism experiment, and cannibalism probably explains why Asynarchus survival was lower than that of Limnephilus survival in the competition experiment. The density independent occurrence in Asynarchus populations suggests that cannibalism in this case might be more related to nutritional supplementation than to population regulation.
IGP, cannibalism, and detritivory
IGP and cannibalism are best documented among aquatic insects with predaceous nymphs (e.g., Odonata: Van Buskirk 1989, Wissinger 1989, Johnson 1991, Johansson 1993, Wissinger and McGrady 1993) and/or predaceous aquatic adults (e.g., aquatic hemiptera: Fox 1975, Sih 1978, Orr et al. 1990 and references therein). In these taxa IGP and cannibalism are often considered to be consequences of relatively indiscriminate foraging behavior (Orr et al. 1990, Johnson 1991). In contrast, limnephilid caddisflies are typically considered detritivores on plant material (Wiggens 1974, 1977, Bariocher et al. 1978, Williams and Williams 1980, Berte and Pritchard 1986), although we found several anecdotal and dietary references that indicate there is an increasing propensity for carnivory during development (Slack 1936, Mecom and Cummins 1964, Winterbourn 1971a, Mecom 1972, Anderson 1976). This tendency has been observed in several other taxa of aquatic detritivores (Winterbourn 1971b, Fahy 1972, Fuller and Stewart 1977, Shapas and Hilsenhoff 1978, Benke and Wallace 1980), and may be more a more general phenomenon than has been previously recognized (Giller and Sangpradub 1993). Our study provides experimental evidence that this shift towards carnivory can include intraguild predation and cannibalism.
Intraguild predators and cannibals face the potential cost of attacking prey that can attack back, and cannibals face the additional risks of disease and parasite transmission, and the potential loss of inclusive fitness from eating kin (Elgar and Crespi 1992). Given these costs, the regular occurrence of these interactions among these caddisflies suggests there must be benefits (Dong and Polis 1992). One hypothesis is that, because IGP and cannibalism result in both an energy gain and the elimination of a potential competitor, these interactions have evolved as an extreme form of interference competition (Johnson et al. 1985, Polis 1988). However, our results suggest that competition for food resources (detritus) is relatively benign at our study site and that IGP and cannibalism occur across a wide range of larval densities.
An alternative hypothesis is that IGP and cannibalism provide these caddisflies with a qualitative dietary supplement. The detritus (spruce needles, wood fragments, aquatic macrophytes) that volumetrically dominates the diet of both species is mainly lignin, cellulose, and hemicellulose (Sparks 1993), has a high carbon to nitrogen ratio, and is probably nutritionally incomplete (Suberkropp et al. 1976, Cummins and Klug 1979, Sinsabaugh et al. 1985, Anderson and Cargill 1987). Carnivory, and specifically IGP and cannibalism, would provide a high-protein and/or lipid supplement that could be necessary for metamorphosis, or at the least, a timely escape from drying habitats (see also Anderson 1976, Iverson 1979, Cargill et al. 1985). The need for such a dietary supplement should be independent of density and especially important under the extremely low nutrient (N, P) conditions and short growing season (see Wissinger and Whiteman 1992) in subalpine and boreal wetlands. Consistent with this hypothesis is the observation that, despite the relatively short-term nature of the first field experiment, Asynarchus pupae were significantly larger in treatments with Limnephilus prey than in those without. Future research on the population consequences of IGP and cannibalism in aquatic insects should focus on quantifying the effects of these interactions on fitness correlates such as time to pupation and emergence, adult size, and adult fecundity.
We thank Alan Carpenter of the Colorado Field Office of The Nature Conservancy and Susan Lohr of the Rocky Mountain Biological Laboratory for facilitating access to the Mexican Cut Nature Preserve. Howard Whiteman, Stephanie Feldhousen, Jill Heimbuch, Darold Batzer, and Andi Craig provided valuable comments on earlier versions of the manuscript. We are grateful to Dan Johnson, Steven Juliano, and an anonymous reviewer for valuable editing, which greatly improved the paper. G. B. Sparks and H. Steltzer were supported by a National Science Foundation (grant BIR-92-0004) Research Education for Undergraduates (REU) site grant to the Rocky Mountain Biological Laboratory. S. A. Wissinger was funded by The Nature Conservancy, Colorado Division of Wildlife, Allegheny College, and a Presidential Young Investigator Award from the National Science Foundation (grant BSR-89-58253).
Anderson, N. H. 1976. Carnivory by an aquatic detritovore, Clistorina magnifica (Trichoptera Limnephilidae). Ecology 57:1081-1085.
Anderson, N. H., and A. S. Cargill. 1987. Nutritional ecology of aquatic detritivorous insects. Pages 903-925 in F. Slansky and J. G. Rodriquez, editors. Nutritional ecology of insects, mites, spiders, and related invertebrates. John Wiley, New York, New York, USA.
Barlocher, F., R. J. Mackay, and G. B. Wiggens. 1978. Detrital processing in a temporary vernal pool in southern Ontario. Archiv fur Hydrobiologie 81:269-295.
Benke, A. C. 1978. Interactions among coexisting predators: a field experiment with dragonfly larvae. Journal of Animal Ecology 47:335-350.
Benke, A. C., and B. Wallace. 1980. Trophic basis of production among net-spinning caddisflies in a southern Appalachian stream. Ecology 65:1-13.
Berte, S. B., and G. Pritchard. 1986. The life histories of Limnephilus externus, Anabolia bimaculata, and Nemotaulius hostilis (Trichoptera: Limnephilidae) in a pond in southern Alberta, Canada. Canadian Journal of Zoology 64:2348-2356.
Cargill, A. S., K. W. Cummins, B. J. Hanson, and R. R. Lowry. 1985. The role of lipids as feeding stimulants for shredding aquatic insects. Freshwater Biology 15:455-464.
Cummins, K. W., and M. J. Klug. 1979. Feeding ecology of stream invertebrates. Annual Review of Ecology and Systematics 10:147-172.
Day, R. W., and G. P. Quinn. 1989. Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59:433-463.
Dodson, S. I. 1970. Complementary feeding niches sustained by size-selective predation. Limnology and Oceanography 15:121-127.
-----. 1974. Zooplankton competition and predation: an experimental test of the size-efficiency hypothesis. Ecology 55:605-613.
-----. 1982. Chemical and biological limnology of six west-central Colorado mountain ponds and their susceptibility to acid rain. American Midland Naturalist 107:1733-1739.
Dong, Q., and G. A. Polis. 1992. The dynamics of cannibalistic populations: a foraging perspective. Pages 12-37 in M. A. Elgar and B. J. Crespi, editors. Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, New York, New York, USA.
Dunson, W. A., and J. Travis. 1991. The role of abiotic factors in community organization. American Naturalist 138:1067-1091.
Ebenman, B., and L. Persson, editors. 1988. Size-structured populations. Springer-Verlag, New York, New York, USA.
Elgar, M. A., and B. J. Crespi. 1992. Ecology and evolution of cannibalism. Pages 1-12 in M. A. Elgar and B. J. Crespi, editors. Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, New York, New York, USA.
Fahy, E. 1972. The feeding behavior of some common lotic insect species in two streams of different detrital content. Journal of Zoology 76:337-350.
Fox, L. 1975. Cannibalism in natural populations. Annual Review of Ecology and Systematics 6:87-106.
Fuller, R. C., and K. W. Stewart. 1977. The food habits of stoneflies in the upper Gunnison River, Colorado. Environmental Entomology 6:293-302.
Giller, P.S., and N. Sangradub. 1993. Predatory foraging behavior and activity patterns of larvae of two species of limnephilid cased caddis. Oikos 67:351-357.
Hurd, L. E. 1988. Consequences of divergent egg morphology to predation and coexistence in two sympatric, congeneric mantids (Orthoptera: Mantidae). Oecologia 76: 547-550.
Hurd, L. E., and R. M. Eisenberg. 1990. Arthropod community responses to manipulation of a bitrophic predator. Ecology 71:2107-2114.
Iverson, T. M. 1979. Laboratory energetics of larvae of Sericostoma personatum (Trichoptera). Holarctic Ecology 2: 1-5.
Johansson, F. 1993. Intraguild predation and cannibalism in odonate larvae: effects of foraging behavior and zooplankton availability. Oikos 66:80-87.
Johnson, D. M. 1991. Behavioral ecology of dragonflies and damselflies. Trends in Ecology and Evolution 6:8-13.
Johnson, D. M., P. H. Crowley, R. E. Bohanan, C. N. Watson, and T. H. Martin. 1985. Competition among larval dragonflies: a field enclosure experiment. Ecology 66:119-128.
Maly, E. J. 1970. The influence of predation on the adult sex ratios of two copepod species. Limnology and Oceanography 15:131-137.
-----. 1973. Density, size, and clutch of two high-altitude diaptomid copepods. Limnology and Oceanography 18:840-848.
Mecom, J. O. 1972. The feeding habits of Trichoptera in a mountain stream. Oikos 23:401-407.
Mecom, J. O., and K. W. Cummins. 1964. A preliminary study of the trophic relationship of the larvae of Brachy-centrus americanus (Trichoptera: Brachycentridae). Transactions of the American Microscopical Society 83:233-243.
Morin, P. J. 1984. Odonate guild composition: experiments with colonization history and fish predation. Ecology 65:1866-1873.
Norusis, M. J. 1990. SPSS/PC=4.0. SPSS, Incorporated. Chicago, Illinois, USA.
Orr, B. K., W. W. Murdoch, and J. R. Bence. 1990. Population regulation, convergence, and cannibalism in Notonecta (Hemiptera). Ecology 71:83-98.
Paine, R. T. 1963. Trophic relationships of eight sympatric gastropods. Ecology 44:63-72.
Park, T. 1954. Experimental studies of interspecific competition II. Temperature, humidity, and competition in two species of Tribolium. Physiological Zoology 27:177-238.
Peckarsky, B. L., and C. A. Cowen. 1991. Consequence of larval intraspecific interference to stonefly growth and fecundity. Oecologia 88:277-288.
Peckarsky, B. L., C. A. Cowan, M. A. Penton, and C. Anderson. 1993. Sublethal consequences of stream-dwelling predatory stoneflies on mayfly growth and fecundity. Ecology 74:1836-1846.
Pimm, S. L. 1978. On feeding on more than one trophic level. Nature 275:542-544.
Polis, G. A. 1981. The evolution and dynamics of interspecific predation. Annual Review of Ecology and Systematics 12:240-255.
-----. 1988. Exploitation competition and the evolution of interference, cannibalism and intraguild predation in age/size structured populations. Pages 183-202 in B. Ebenmen and L. Persson, editors. Size-structured populations. Springer-Verlag, New York, New York, USA.
Polis, G. A., and R. D. Holt. 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends in Ecology and Evolution 7:151-155.
Polis, G. A., C. Myers, and R. D. Holt. 1989. The ecology and evolution of intraguild predation, potential competitors that eat each other. Annual Review Ecology and Systematics 20:297-330.
Shapas, T. J., and W. L. Hilsenhoff. 1978. Feeding habits of Wisconsin's predominant lotic Plecoptera, Ephemeroptera, and Trichoptera. Great Lakes Entomologist 9:269-311.
Sih, A. 1978. Foraging strategies and the avoidance of predation by an aquatic insect, Notonecta hoffmani. Ecology 63:786-796.
Sinsabaugh, R. L., A. E. Linkings, and E. F. Benfield. 1985. Cellulose digestion and assimilation by three leaf-shredding aquatic insects. Ecology 66:1464-1471.
Skelly, D. A., and E. E. Werner. 1990 Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:1213-2322.
Slack, H. D. 1936. The food of caddisfly (Trichoptera) larvae. Journal of Animal Ecology 5:105-115.
Sparks, G. B. 1993. Competition and intraguild predation between two species of caddisfly (Trichoptera) larvae in permanent and semi-permanent high elevation ponds. B.S. Thesis. Allegheny College, Meadville, Pennsylvania, USA.
Spiller, D. A., and T W. Schoener. 1990. Lizards reduce food consumption by spiders: mechanisms and consequences. Oecologia 83:150-161.
Sprules, W. G. 1972. Effects of size-selective predation and food competition on high altitude zooplankton communities. Ecology 53:375-386.
Suberkropp, K. F., G. L. Godshalk, and M. J. Klug. 1976. Changes in the chemical composition of leaves during processing in a woodland stream. Ecology 57:720-727.
Van Buskirk, J. 1989. Density-dependent cannibalism in larval dragonflies. Ecology 70:1442-1449.
Ward, J. V. 1992. Aquatic insect ecology: 1. Biology and habitat. John Wiley and Sons, New York, New York, USA.
Warner, S. C., J. Travis, and W. A. Dunson. 1993. Effect of pH variation on interspecific competition between two species of hylid tadpoles. Ecology 74:183-194.
Werner, E. E., and J. F. Gilliam. 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics 15:393-425.
Whiteman, H. H., S. A. Wissinger, and A. Bohonak. 1994. Seasonal movement patterns and diet in a subalpine population of the tiger salamander, Ambystoma tigrinum nebulosum. Canadian Journal of Zoology 72:1780-1787.
Whiteman, H. H., S. A. Wissinger, and W. S. Brown. 1996. Growth and foraging consequences of facultative paedomorphosis in the tiger salamander, Ambystoma tigrinum nebulosum. Evolutionary Ecology 10:429-422.
Wiggins, G. B. 1973. A contribution to the biology of caddisflies (Trichoptera) in temporary pools. Life Science Contributions of the Royal Ontario Museum 88:1-28.
-----. 1977. Larvae of North American caddisflies (Trichoptera). University of Toronto Press, Toronto, Ontario, Canada.
Wilbur, H. M. 1984. Complex life cycles and community organization in amphibians. Pages 195-224 in P. W. Price, C. N. Slobodchikoff, and W. S. Gaud, editors. A new ecology: novel approaches to interactive systems. John Wiley and Sons, New York, New York, USA.
-----. 1988. Interactions in size-structured populations: from individual behavior to ecosystem dynamics. Pages 157-170 in B. Ebenman, and L. Persson, editors. Size-structured populations. Springer-Verlag, New York, New York, USA.
Wilbur, H. M., and R. A. Alford. 1985. Priority effects in experimental pond communities: responses of Hyla to Bufo and Rana. Ecology 66:1106-1114.
Williams, N. E., and D. D. Williams. 1980. Distribution and feeding records of the caddisflies of the Matamek River region. Canadian Journal of Zoology 57:2402-2412.
Winterbourn, M. J. 1971a. The life histories and trophic relationships of the Trichoptera of Marion Lake, British Columbia. Canadian Journal of Zoology 49:623-635.
-----. 1971b. An ecological study of Banksiola crotchi Banks (Trichoptera: Phyrganeidae) in Marion Lake, British Columbia. Canadian Journal of Zoology 49:636-645.
Wissinger, S. A. 1988. Spatial distribution, life history, and larval survivorship in a 14-species assemblage of larval dragonflies (Odonata:Anisoptera). Freshwater Biology 20:329-340.
-----. 1989. Seasonal variation in the intensity of competition and intraguild predation among dragonfly larvae. Ecology 70:1017-1027.
-----. 1992. Niche overlap and the potential for competition and intraguild predation in size-structured populations. Ecology 73:1421-1444.
Wissinger, S. A., and J. McGrady. 1993. Intraguild predation and competition between larval dragonflies: direct and indirect effects on shared prey. Ecology 74:207-218.
Wissinger, S. A., and H. H. Whiteman. 1992. Fluctuation in a Rocky Mountain population of salamanders: anthropogenic acidification or natural variation? Journal of Herpetology 26:377-391.
|Printer friendly Cite/link Email Feedback|
|Author:||Wissinger, Scott A.; Sparks, Grace B.; Rouse, Gretchen L.; Brown, Wendy S.; Steltzer, Heidemarie|
|Date:||Dec 1, 1996|
|Previous Article:||Egg limitation, host quality, and dynamic behavior by a parasitoid in the field.|
|Next Article:||Facultative mutualism between red mangroves and root-fouling sponges in Belizean mangal.|