Although only a small number of terrestrial insect species have aquatic developmental stages, these larvae compose a large portion of the macroinvertebrate biomass found in most aquatic ecosystems. In some systems, caddisfly larvae (Trichoptera) constitute a substantial portion of this biomass. Aquatic insect forms demonstrate an immense array of behavioral and physiological adaptations to successfully occupy a given habitat. Many larval Trichopteran species have evolved the ability to build a mobile case which serves as a primary, mechanical defense against both vertebrate and invertebrate predators. These tubular cases are constructed from silk and debris and display a high amount of species-specific construction. Both generalized and specialized crypsis occur in case construction depending on habitat type. Many species utilize fine substrate particles (sand and organic detritus) to mimic their average habitat type. Other species, however, may employ hollowed plant material to mimic specific detritus. It has been shown that vertebrate predators prefer non-cased larvae over case-building species, however, there is also predator selection among cased larvae. For this reason, there is a high amount of intra-species competition among Trichopteran larvae for non-predator-selected cases. Cases have also been shown to act as foraging and respiratory devices and to aid in the resistance of entry into stream drift. Case-building species, therefore, may have an advantage in occupying feeding patches and habitats that non-case-building species would not inhabit for the risk of predation. Thus, case-building caddisfly species have developed a defense suitable for aquatic environments that allows them to utilize optimal microclimates which other non-case-building species cannot because of predation pressures.
Introduction
Although only a small number of terrestrial insect species have aquatic developmental stages, these larvae compose as much as 95% of the macroinvertebrate biomass found in some aquatic systems (Ward, 1992). Aquatic insect forms have, therefore, developed an immense array of behavioral and physiological adaptations to successfully occupy a diverse range of habitats (Merritt and Cummins, 1984). Caddisfly larvae (Trichoptera) sometimes comprise a large portion of this macroinvertebrate biomass. Species of Trichoptera occur on every continent except Antarctica and consist of about 10,000 species worldwide. 1200 species occur in North America alone (Ward, 1992).
Although life histories among Trichopterans are diverse (Merritt and Cummins, 1984), most are holometabolous and have aquatic larvae and pupae, and terrestrial adults. Univoltinism is most common, however, some species complete more than one generation per year while others require two years for development (Peckarsky 1990).
Caddisflies, like most other aquatic insects, probably evolved in cold, fast-flowing environments (Peckarsky, 1990; Mackay and Wiggins, 1979), but quickly colonized both lentic and lotic systems due to subsequent morphological adaptations. Trichoptera are a sister group of Lepidoptera (Mackay and Wiggins, 1979) and also can produce silk. Silk production probably supported rudimentary case and net-spinning construction in early Trichopterans which allowed exploitation of habitats with otherwise unfavorable conditions. This silk production has contributed to the diversification of feeding habits, defensive capabilities, and microhabitat selection.
Five groups within the three superfamilies of Trichoptera have been identified based on case-building behavior alone (Peckarsky 1990). This behavior has enhanced defensive capabilities which has allowed subsequent improvements in habitat selection and ecological diversity. Case-building behavior is usually species-specific although construction may vary depending upon available habitat. Cases function as ballast camouflage, and mechanical defenses (Peckarsky 1990).
The ability of larval Trichopterans, therefore, to construct cases from silk and surrounding materials has led to their ecological diversification and utilization of habitats unavailable to other aquatic macroinvertebrates.
Discussion
Case Building Behavior
Material and Ontogeny
Probably the most important aspect of ecological diversity among Trichopterans is the ability to produce silk. Silk production has enabled caddisflies to exploit a wide range of aquatic habitats. Silk utilization is different in most families and has more or less defined the ecological role of caddisflies. According to Mackay and Wiggins (1979), three modes of existence have resulted from silk utilization. Some families such as the caseless, predatory Rhyacophiloidea spin only a thin thread while moving along the substrate. Other more sedentary larvae such as the Hydropsychoidea spin nets or fixed shelters which serve as food capture devices. The third, and probably most significant utilization of silk production is the construction of mobile cases by such families as the Limnephiloidea.
Most case-building species construct cases of material from their immediate surroundings. Otto (1980) divides case construction into organic and mineral groups. The case size, shape, and material choice are usually species-specific although some modification may occur due to limited resource availability. This availability may determine the quantity and quality of building material in some species and may impose a preferential sequence if the material is limited (Hansell, 1972; Otto, 1980).
In addition, many species demonstrate an ontogenic association with case-building and material. Upon hatching, early instar larvae of case-building species immediately initiate case construction. It has been demonstrated (Otto, 1987 b; Rowlands and Hansell, 1987) that caseless larvae preferentially preyed upon more than cased individuals and avoided both cased and uncased Trichopteran larvae. Selection of initial construction material varies from species to species although many demonstrate a preference for certain resources. Although initial building material may be produced from a certain resource, many Trichopterans such as Lepidostoma hirtum may change building strategies during larval development (Hansell, 1972). L. hirtum constructs a tubular, sand grain case immediately upon hatching, however, building material abruptly changes from mineral to vegetative resources during the 3rd instar. This behavior has also been observed in other species (Anderson, 1980; Elliot, 1970; Otto, 1980; Rowlands and Hansell, 1987). This change in resources, however, may differ among species i.e. mineral to vegetative or vegetative to mineral.
One obvious reason for this transition is resource availability. Many species alter their construction material when a more valuable or abundant resource becomes practical. A larger number of summer species make cases from mineral resources as compared with autumn species which show a predominance of organic cases fashioned from fallen leaves (Otto, 1980).
Consequently, different species relying on similar building materials may occupy the same habitat by developing temporal niches to avoid strict competition for resources (Mackay and Wiggins, 1979). Species with distinct developmental rates may segregate resources by utilizing them at different times when others have either completed or just begun their development and do not require similar items. This allows for optimal utilization of mineral and vegetative resources by multiple species.
Competition and Energetics
Inter- and intra-species competition for cases and case material, however, does occur (Otto, 1980; Otto, 1987a; Otto, 1987b). Specific case shapes, sizes, and compositions are seemingly in demand. Otto (1974) estimates that the energetics of silk production in Trichopterans amounts to about 12% of the total energy content of the larvae. Consequently, this energy expenditure may be considerable in less productive systems.
Larvae seem to prefer building material that involves the least amount of energy investment without compromising necessary aspects of predator avoidance and movement over the substrate. Case construction and selection of Agrypnia pagetana illustrates these energetic trade-offs (Otto, 1987b). A. pagetana constructs cases from small vegetative material or alternately uses a natural hollow stem. Energetic costs of silk production in vegetative cases are high compared to the use of hollow stems which require only a silk lining. If hollow stems are not readily available, however, an early instar larvae will construct a vegetative case. Because of the higher energy investment allocated towards the construction of vegetative cases, they are not as readily abandoned or captured by another larva as compared with hollow stem cases (Otto, 1987b). Therefore, owners of vegetative cases will strongly defend their past energy investment against opponents while hollow stem owners readily surrender their cases. Owners of hollow stem cases more than 2 days old will voluntarily exchange the old case for a new, more rigid stem if one is encountered (Otto, 1987b).
In Potamophylax cingulatus the transition of case material from leaf discs to mineral resources may be due to energetic tradeoffs of early development (Otto, 1980). The use of abundant leaf discs by early instar larvae during certain times of the year is less costly than the silk requirement for constructing mineral cases. This allows P. cingulatus to assimilate more energy for early growth. In addition, the use of more resistant mineral cases may be advantageous to larger, later instar larvae which have a greater probability of predation by vertebrate predators.
These energetic tradeoffs in early developmental stages may, therefore, conserve energy required for later predator avoidance, pupation, and reproduction. Consequently, the energetic cost of case materials may ultimately affect future fecundity.
Predator Avoidance
Crypsis
Although these examples demonstrate the relative costs and benefits of case construction throughout larval development, the most apparent, although sometimes disputed (Williams, 1987), the purpose of case construction in Trichopteran larvae is defense and prey avoidance.
Because building material is obtained from the immediate surroundings, larvae, in most cases, are naturally camouflaged against the surrounding habitat. Cryptic defense, therefore, is inherent in case construction. Larvae that construct mineral cases are more likely to be preyed upon if they stray onto a vegetative substrate (Otto, 1980). It is likely then, that larvae maintain a home range upon substrate which resembles its particular case construction to avoid predation.
Resistance to Accidental Drift
In addition, many lotic aquatic insect species, including caddisflies, inhabit microhabitats which expose the larvae to extremes of current velocity. Although stream drift is a typical mode of dispersal for many aquatic larvae, accidental entry may occur. A strong current may dislodge larvae from the substrate to the drift where they are more likely to be consumed by predators. Case design may impede or completely prevent accidental entry into the current drift of lotic systems (Waringer, 1989). Waringer (1989) has shown that stone cases are most effective on gravel substrates, however, are less effective on vegetative or sandy bottoms. The same reasoning applies to vegetative cases although to a lesser extent. While significantly heavier stone cases may offer added weight in high flow conditions and limit accidental displacement, the energetics of producing and carrying these titanic dwellings are not reasonable for an average species. A resistance coefficient of 0.8 has been calculated for cylindrical, smooth stone cases while an average, streamlined body has an approximate value of 0.05 (Waringer, 1989).
Although case material increases the amount of drag forces incurred, it is probably more beneficial for early instar larvae and smaller species that lack the strength to adhere to the substrate during high current velocities. It has been shown that larger, caseless larvae are not dislodged until current velocities reach 2 ms-1. Although this is almost twice the current resistance of case-building species (Waringer, 1989) most smaller species lack the physical strength to resist these high-flow conditions. Therefore, case development as a means of preventing accidental displacement from the substrate is advantageous in smaller species.
Predator Affects and Microhabitat Distribution
Microhabitat distribution and predator avoidance is probably the most significant aspect of case-building behavior in Trichopteran larvae. Case construction allows for crypsis and mechanical protection. Tinbergen (1967), however, points out that camouflage is only effective if accompanied by specific types of behavior. Thus, larval Trichoptera utilize microhabitat distribution, temporal niche selection, and defense behavior, in addition to case construction, as a means of avoiding predation and optimizing food and habitat resources.
Case construction material seems to have an overall effect on predator attack, capture, and ingestion (Johansson, 1991). Although mineral cases seem to have a higher crushing resistance to vertebrate predation than some vegetative cases, this may not offer an overall advantage (Otto, 1980). Predators are assumed to determine prey choice by the minimal amount of handling and search time that would maximize the energy per unit of foraging time (Pyke et al, 1977). Many mineral-cased larvae are readily preyed upon by vertebrate predators, however, are ejected shortly thereafter because of the difficulties of breaching the resistant case (Johansson, 1991). Certain sizes and shapes of vegetative cases, however, are equally difficult to handle due to added protuberances or long case lengths (Johansson, 1991).
One would assume that selective pressure would favor those individuals who construct heavy, structurally sound cases that offer significant crushing resistance. Mineral cases, although providing an excellent mechanical defense, are energetically costly to construct and maintain. Many vegetative cases, however, provide a greater amount of cryptic defense while providing similar mechanical capabilities along with less energy expenditures. Longer-cased species exhibit an overall advantage to predator avoidance when compared to those constructing short cases (Johansson, 1991) due in part to the difficulty of ingestion by vertebrate predators.
Case rigidity is of little benefit if parts of the larva are exposed to predators. This, however, may be of little importance to invertebrate predators such as larval Dytiscus spp. (Coleoptera). The relative size and aggressive behavior of these and other invertebrate predators allows for rapid extraction of cased Trichopteran larva. The relative handing time of cased Trichopteran larvae by Dytiscus spp. is considerably more than that of vertebrate predators (Johansson, 1992). In most cases, Dytiscus spp. will simply wait for the apprehended larva to expose a portion of itself beyond the protective confines of the case. Case design does, however, show some resistant adaptations to this predation (Johansson, 1992).
Many species have also developed behavioral adaptations to augment the defensive character of case construction. It is assumed that Trichopteran larvae do not purposely make themselves conspicuous to predators unless accidentally displaced from their normal habitat. Since most larvae can only recognize predators by direct contact, the chances of avoiding predation in a different habitat are small (Johansson, 1991). Larval movement has proved to be the best predictor of risk for macroinvertebrates to predation by vertebrate predators (Ware, 1973). Many benthic feeders rely almost exclusively on sight to locate food. Johansson (1991) has shown that immobile larvae stand a better chance of predator avoidance under these conditions. Some species feign death longer than others if the threat of predation persists (Johansson, 1991). Once again, this amount of death feigning may be a function of the relative case strength. Potamophylax cingulatus exhibits only a small amount of death-feigning behavior due to its rigid case which offers adequate protection (Johansson, 1991).
All of these defensive behavioral adaptations have allowed Trichopteran larvae to optimize the microhabitat distribution of the aquatic environments that they inhabit. Habitat selection by aquatic insects is crucial due to the amount of variability normally encountered in aquatic environments (Statzner, 1981). Many aquatic insect species, including some Trichopterans (Elliot, 1970), exhibit diel fluctuations in habitat selection which affords better refuge from predators. Some species of Plecopterans, Ephemeropterans, and other insects that lack similar forms of primary defensive capabilities exhibit negative phototactic responses (Ward, 1992) and favor undersides of stones and gravel during diurnal periods to escape predation. During these increased times of predation, however, many case-building Trichopteran species are abundant on substrate surfaces where food availability is high (Koetsier, 1989; Personal Observation). Although studies have shown that vertebrate predation alone does not significantly decrease the overall density of aquatic insects, cased Trichopterans do seem to have an advantage in some situations (Allan, 1982; Koetsier, 1989).
Exposed rock surfaces provide better foraging for grazer species utilizing periphyton communities as a food source. These exposed surfaces increase available light energy for primary production (Steinman and McIntire, 1986) and provide rich feeding patches for Tichopteran grazers. Although periphyton growth itself affords some amount of refuge for invertebrate grazers, the advantage of case construction under these exposed conditions cannot be discounted. In addition, lotic net-spinning caddisflies are usually not evenly distributed along a watercourse (Otto, 1985) and instead aggregate in areas of high resource availability. These rich patches, however, are usually more risky because of their increased exposure to predation. Catch-net constructing species usually inhabit downstream reaches of lotic environments where fish are regularly encountered. Because nets are usually constructed in exposed areas where drift is easily accessible, case-building species may have an advantage over non-case builders. These strategies allow Trichopteran larvae to utilize rich feeding patches which other macroinvertebrates find too risky. Exposed substrate surfaces offer productive feeding opportunities for grazers and net-spinning species. Case construction, therefore. allows for colonization and utilization of rich microhabitats that are otherwise inaccessible to most macroinvertebrates.
Conclusions
Ecological diversification is important to the survival of any organism and behavioral adaptations are the basis for many successful taxa which have succeeded in colonizing numerous habitats. Case-building behavior of caddisfly larva is an obvious advantage in most circumstances. Resource and habitat acquisition is facilitated by the mechanical and cryptic defensive applications of larval cases. The construction of portable cases has enabled some caddisfly larvae to avoid otherwise considerable predation pressures which may prevent colonization and utilization of certain resources. Intense competition for sufficient resources in aquatic environments has enabled caddisflies to evolve a means of directly occupying more suitable habitats. This acquisition of rich resources has extended the habitat of Trichopterans to a variety of aquatic environments.
Case construction may contain a complex succession of behaviors that allow species-specific adaptations that further habitat utilization, predator avoidance, and ultimately reproductive success.
Case-building in caddisfly larvae, therefore, is a considerable advantage for those species that utilize this behavior.
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