Research Article |
Corresponding author: John C. Morse ( jmorse@clemson.edu ) Academic editor: Wolfram Graf
© 2023 Megan J. Bishoff, Lang Peng, Hao-ming Zang, John C. Morse.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Bishoff MJ, Peng L, Zang H-m, Morse JC (2023) Defensive phragmosis and cathaptosis in Trichoptera larvae. Contributions to Entomology 73(2): 209-218. https://doi.org/10.3897/contrib.entomol.73.e110394
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Phragmosis, or the use of specially modified body parts and associated behaviors to block an opening as defense against predators, is a commonly observed phenomenon in certain ants and termites that block entrances of their subterranean nests with large, flat heads. It has been reported in some beetles and other insects and even in some frogs. Common features of phragmosis in caddisfly larvae include a hard and usually flat body surface, with or without stout spines, and the behavior of fitting that body surface tightly in the opening of its case. A different defensive strategy occurs in snails and case-making larvae of camptosomate leaf beetles (Chrysomelidae: Cryptocephalinae and Lamprosomatinae) that protect themselves from predators by securing the openings of their shells or cases firmly against the substrate, a behavior we call “cathaptosis.” Common features of cathaptosis in caddisfly larvae include a case with its vulnerable opening oriented parallel with the substrate and accompanied by behavior that grips the substrate, fixing the case opening firmly against it when threatened. We suggest that these defensive strategies have evolved multiple times in Trichoptera, especially in case-making larvae. We demonstrate some examples and provide tentative lists of caddisflies whose larvae may have evolved these defensive strategies.
behavior, case, cover, evolution, predator, shield
A “chokepoint” is an important strategic passage through an otherwise impassible territory, usually substantially narrower than that territory, which greatly decreases the advantage of a superior attacker. In a military context, King Leonidas I’s leadership of the Spartans to defend the narrow Pass of Thermopylae during the Persian invasion of Greece, led by Xerxes I on 21 August 480 BCE, serves as an historic example. “Phragmosis” (from φράγμα, pronounced “frágma,” meaning “barrier” or “shield”) is a similar evolutionary strategy that integrates a specialized morphology (shield) and a corresponding behavior to defend a narrow opening (chokepoint) by a single individual or small group of individuals, described originally for the structure and behavior of certain species of soil-nest-building, colonial ants (
Alternatively, some encased animals defend the chokepoint opening of a portable case or shell by pressing it against impenetrable substrate. Such a case or shell has only one opening and the shape of that opening conforms to the shape of the impenetrable substrate. The encased animal may also have adaptations that help it to hold itself especially tightly against the substrate. We term this structure and behavior “cathaptosis” (from καθάπτω, pronounced katháptō, meaning to fasten or make fast) to describe the behavior of grasping the substrate firmly and holding it tightly against the shell or case opening. Does this phenomenon also occur in at least some case-bearing caddisflies?
In the family Hylidae, a tree frog Corythomantis greeningi Boulenger, 1896 has a phragmotic head (including the eyelids) with flat, rough, and venomous properties (
The casque-headed tree frog Corythomantis greeningi Boulenger, 1896 (Hylidae) (from
Some arachnids are phragmotic. For example, trapdoor spiders are known to create a tunnel in the ground, coating it with silk, and giving it a tightly fitting cover or “door” made of silk and debris. Some trapdoor spiders, in genera such as Cyclocosmia Ausserer, 1871 (Fig.
Among eusocial groups, soldiers or workers of some ants (Formicidae) have phragmotic heads and behaviors (
Other ants have evolved unique approaches for employing phragmotic defense. For example, a rare cooperative phragmotic defense has been reported in the genus Cephalotes Latreille, 1802 (Formicidae). Several workers and/or soldiers, depending on the species, collectively use their phragmotic heads to block large or irregular nest openings by having multiple ants assemble and obstruct the opening with a multi-organismal wall (
Phragmosis and camouflage examples. A. Diagram of nest and queen of Blepharidatta canops Kempf, 1967 (Formicidae: Myrmicinae) using head and pronotum to block brood chamber (
Some ants also use camouflage in conjunction with phragmosis. The phragmotic head of some Cephalotes species commonly accumulates dirt in the shallowly concave disk (
Some Coleoptera also defend themselves with phragmosis. Keyhole ambrosia beetles such as Amasa truncata (Erichson, 1842) (Curculionidae) have truncate elytra forming a flat circular posterior (
In these examples from terrestrial animals, a flattened and hardened anterior or posterior surface has evolved as defense against predation. We hypothesized that a similar phenomenon may have occurred in another group of animals that defends a small opening, the larvae of case-bearing Trichoptera. Larvae of various tube-case-making caddisflies in subterorder Phryganides construct many particular shapes of cases using silk and a wide variety of building materials assembled in characteristic patterns. These cases have evolved for camouflage, physical protection, and as a respiratory aid (
Furthermore, our hypothesis is that phragmosis has evolved independently in a variety of Trichoptera genera along different evolutionary pathways either alone or possibly in conjunction with filter feeding or other adaptations. Examples of species that may exhibit phragmosis in Trichoptera include at least those in Table
Selected Trichoptera species with morphological shields that may be phragmotic.
Family | Species | Case | Phragmotic surface (shield) | Habitat | Food/ feeding method | References illustrating shield |
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Apataniidae | Allomyia scotti Wiggins, 1973 | Small stones | Head (with horns) | Lotic-erosional, hygropetric | Periphyton/scraper |
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Apatania theischingerorum Malicky, 1981 | Small stones | Head | Lotic-erosional | Periphyton/scraper |
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Antipodoeciidae | Antipodoecia turneri Mosely, 1934 | Small stones | Head + pronotum | Lotic-erosional | Unknown |
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Anomalopsyche minuta (Schmid, 1957) | Small stones | Head + pronotum | Lotic erosional | Periphyton/scraper |
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Beraeidae (Wallengren, 1891) | Beraeamyia squamosa Mosely, 1930 | Small stones | Head | Lotic-erosional | Unknown |
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Beraea fontana Wiggins, 1954, etc. | Small stones | Head + pronotum | Eucrenon muck (argyllal) | Fine Particulate Organic Matter (FPOM)/ gatherer |
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Beraeodes minutus (Linnaeus, 1761) | Small stones | Head | Variable | Periphyton/Scraper |
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Brachycentridae | Brachycentrus americanus Banks, 1899 | Plant material | Head | Lotic-erosional | FPOM & prey/filterer, periphyton/scraper |
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Brachycentrus maculatus (Fourcroy, 1785) | Fine sand | Head | Lotic-erosional | FPOM, prey, periphyton/filterer, predator, scraper, gatherer |
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Dolichocentrus sakura Nozaki, 2017 | Fine sand | Head | Lotic-erosional, -depositional | Unknown |
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Micrasema rickeri Ross & Unzicker, 1965 | Plant material | Head | Lotic-erosional | Mosses/shredder |
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Micrasema minimum McLachlan, 1876, etc. | Fine sand | Head | Lotic-erosional | Mosses, periphyton/shredder, scraper |
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Tsudaea kitayamana (Tsuda, 1942) | Sand grains with moss attached | Head | Lotic-erosional | Mosses/shredder |
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Goeridae | Goera rupicola Nozaki & Shimura, 2020 | Small stones & larger ballast stones | Head + pronotum + mesonotum | Lotic-erosional rock surface (hygropetric) | Periphyton/scraper |
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Goera calcarata Banks, 1899 | Small stones & larger ballast stones | Head | Lotic-erosional rock surface | Periphyton/scraper | Flint 1960 | |
Goeracea genota Ross, 1941 | Small stones & larger ballast stones | Pronotum + mesonotum | Lotic-erosional | Periphyton/scraper |
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Lepania cascada Ross, 1941 | Small stones | Head + pronotum + mesonotum | Organic muck of springs | FPOM/gatherer |
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Silo pallipes (Fabricius, 1781), etc. | Small stones & larger ballast stones | Head + pronotum + mesonotum | Lotic-erosional | Periphyton/scraper |
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Lithax obscurus (Hagen, 1859), etc. | Small stones & larger ballast stones | Head + pronotum + mesonotum | Lotic-erosional | Periphyton/scraper |
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Larcasia akagiae Nishimoto & Tanida, 1999 | Small rock fragments | Head (with knobs) | Lotic-erosional | Periphyton/scraper |
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Lepidostomatidae | Lepidostoma emarginatum (Ito, 1985) | Leaf panels | Head | Springbrooks | Coarse Particulate Organic Matter (CPOM)/shredder-detritivore |
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Theliopsyche melas Edwards, 1956 | Fine sand | Head | Springbrooks | Unknown |
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Leptoceridae | Setodes incertus (Walker, 1852), etc. | Coarse sand | Abdominal segment X | Burrowing in lotic sand | FPOM, prey/gatherer, predator |
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Limnephilidae | Cryptochia pilosa (Banks, 1907) | Wood | Head | Wet riparian wood, leaves | CPOM/shredder-detritivore |
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Cryptothrix nebulicola McLachlan, 1867 | Sand | Head | Lotic-erosional | Prey/filtering predator |
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Drusus chrysotus (Rambur, 1842) | Sand | Head | Lotic-erosional | Prey/filtering predator |
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Ecclisopteryx madida (McLachlan, 1867) | Sand | Head + pronotum | Lotic-erosional | Periphyton/scraper |
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Limnephilus extricatus McLachlan, 1865 | Sand | Abdominal segment X | lentic | CPOM, prey, periphyton/shredder, predator, scraper |
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Rossianidae | Rossiana montana Denning, 1953 | Coarse sand | Head + pronotum | Springbrooks, hygropetric | Woody debris, fungi/gouger, shredder |
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Sericostomatidae | Fattigia pele (Ross, 1938) | Fine sand | Head | Burrowing in sand of springbrooks | FPOM/gatherer |
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Notidobia ciliaris (Linnaeus, 1761) | Fine sand | Head | Burrowing in sand, springbrooks to streams | CPOM/shredder |
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We think the three necessary criteria for phragmosis are as follows: (1) there must be a small entryway to be defended, (2) the morphology of the phragmotic shield should correspond with the shape of that entryway, and (3) the phragmotic shield must be deployed in the entryway whenever an intruder attacks or threatens to attack. Although phragmosis was originally proposed as a strategy to defend a stationary opening to an underground nest (
To test this phragmosis hypothesis, we needed to observe the third criterion, the actual use of an apparent shield by a case-making caddisfly larva to block its opening when disturbed by a predator.
In our pursuit of examples of caddisfly phragmosis we suspected another type of defense designed to protect the opening of a portable and otherwise protective dwelling. We define “cathaptosis” as any method by which an animal defends itself at a vulnerable opening of such a portable case or shell by holding the substrate tightly against the opening. This behavior has been previously described for case-bearing larvae of camptosomate leaf beetles such as Neochlamisus gibbosus (Fabricius, 1777; as Arthrochlamys plicata Fabricius, 1798) and Exema canadensis Pierce, 1940 (both Chrysomelidae: Crytocephalinae) (
Unlike phragmosis, this defense does not require a specialized flattened morphological adaptation, although some beetle species do have flattened heads to press against the substrate. An example of cathaptosis in animals other than insects is freshwater pulmonate snails (Pulmonata). These gastropods use their slime and foot as a suction disk to grip the substrate. When attacked, the snail draws itself into its shell, causing difficulty for a predator to lift the shell from its substrate to access the soft-bodied snail (personal observation).
In both beetles and snails, the animals have developed a method with which to gain a purchase on their substrate sufficient to defend themselves within their protective, portable cases. We think the three necessary criteria for cathaptosis are as follows: (1) there must be a protective, portable case or shell with an entryway to be defended; (2) the morphology of the case and its opening should correspond with the shape of the substrate surface on which the animal lives; and (3) when an intruder attacks or is threatening, the entryway must be sealed by the animal holding the entryway tightly against the substrate.
Unlike case-bearing leaf beetles, for which the case opening is often transverse with the length of the case, case-bearing caddisflies living in lotic waterways must carry their cases horizontal with the flow of the water in a manner that provides least resistance to the water. Therefore, to meet the second criterion, the opening of a case of a stream-dwelling caddisfly larva with cathaptotic behavior will be usually oblique (or beveled) or ventral to apply against the substrate most effectively. We propose that case-making Trichoptera larvae living in streams on exposed substrates and with beveled or ventral anterior case openings, such as those listed in Table
Selected Trichoptera species with cases that may be used in cathaptosis.
Family | Species | Case | Anterior case opening | Habitat | Food/ feeding method | References illustrating case |
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Apataniidae | Apatania arizona Wiggins, 1973 | Rock fragments | Oblique (final instar) | Springbrooks, lakes | Periphyton/scraper |
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Calamoceratidae | Anisocentropus pyraloides (Walker, 1852) | Two dead leaves | Ventral | Lotic-depositional, in debris, on rocks (final instar) | Coarse Particulate Organic Matter (CPOM)/shredding detritivore |
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Heteroplectron californicum McLachlan, 1871 | Excavated stick | Oblique | Lotic- depositional, in debris & on wood | CPOM/shredding detritivore |
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Glossosomatidae | Glossosoma intermedium (Klapálek, 1892) | Rock fragments | Ventral | Lotic-erosional, on rocks | Periphyton/scraper |
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Helicopsychidae | Helicopsyche borealis (Hagen, 1861) | Sand grains | Ventral | Lotic, lentic | Periphyton/scraper |
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Leptoceridae | Ceraclea ancylus (Vorhies, 1909) | Fine sand | Oblique | Lotic depositional, on rocks | Periphyton/scraper |
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Molannidae | Molanna flavicornis Banks, 1914 | Rock fragments | Ventral | Lotic-depositional, lentic | Periphyton, Fine Particulate Organic Matter (FPOM), prey/scrapers, gatherers, predators |
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To test this cathaptosis hypothesis, we needed to observe the third criterion, the actual fastening of a case to substrate by a case-making caddisfly larva to block its opening when disturbed by a predator.
To test our hypothesis for phragmosis, we observed the predator-prey interaction of case-making larvae of two Trichoptera species found locally in the Southern Appalachian Mountains when confronted with predators common in their habitats. The larva of Goera calcarata Banks, 1899 (Goeridae) makes a tubular case with lateral ballast stones for stability in fast-flowing water as it scrapes periphyton from the top surfaces of rocks in lotic-erosional habitats (
Mature larvae of G. calcarata were collected from the tops of stones in a first-order stream at 34°45.366'N, 82°51.372'W, ca. 300 m a.s.l., and young larvae of F. pele were sifted from sand in a springbrook at 35°22.2'N, 83°6.6'W, ca. 1,520 m a.s.l. Available predators at those sites included larvae of Acroneuria abnormis (Newman, 1838) (Plecoptera: Perlidae) and Corydalus cornutus (Linnaeus, 1758) (Megaloptera: Corydalidae). Specimens of both the Trichoptera and the predators were transported back to the laboratory with stream water in separate plastic bags on ice and were kept alive and starved in refrigerated stream water until their interactions could be documented a few days later.
The observation arena was a wide glass dish filled with stream water. A caddisfly and a predator were introduced into the arena and observed for a few minutes as they warmed to room temperature. We observed and recorded the interactions through a Celestron Microscope Pro® Model #44308 attached to a computer.
To test our hypothesis of cathaptosis, we observed the case and behavior of a Chinese species of Ascalaphomerus Walker, 1852 (Calamoceratidae). Larvae of an Ascalaphomerus species were captured on pieces of wood in a pool of a mountain creek (P.R. China: Zhejiang Province, Li-shui City, Yun-he County, Dian-qing-shan Village, Yun-tan-xi Stream 28°9.72'N, 119°41.532'E, ca. 320 m, 9 August 2022) and brought with the wood to the laboratory for testing. Leaf litter, stones, and woody debris (twigs) were placed with the larvae in a rearing chamber. Instead of using a living predator, we gently agitated a test animal with a probe. The response of the larva was recorded with an Olympus TG-6 digital camera (Olympus, Beijing, China).
For the experiment to test for phragmosis when disturbed by a stonefly or hellgrammite predator, each of the larvae of F. pele and G. calcarata quickly withdrew into its case to expose only the flattened front of the head (F. pele) or flattened top of the head and anterior nota (G. calcarata), behavioral responses consistent with phragmosis. This activity was recorded (
For the experiment to test for cathaptosis, an Ascalaphomerus specimen responded to the probing activity by gripping the piece of wood tightly and pressing the case opening onto the wood. The larva also spun silk to anchor the lower edge of the case even more securely to the wood. This activity and the silk anchor were recorded (
Recent studies have demonstrated that flat-headed structure in some Drusus species (Limnephilidae) is adapted to the creation of vortices for entrapping prey (
However, larvae with flat heads also live in a wide variety of other habitats and feed with various other methods on a wide range of food resources. For example, caddisflies with flat, apparently phragmotic structure inhabit not only fast-flowing water, but also organic muck, drifting sand, hygropetric habitats, or quiet pools with accumulations of organic debris (Table
Interestingly, there are also examples of flattened heads in some retreat makers of the suborder Annulipalpia. The larvae of at least some species of Macrostemum (Hydropsychidae) have flat heads that a larva may use to block the anterior opening of the side channel of its highly specialized retreat or to help direct the flow of water through its filternet, or both.
For the experiment to test for cathaptosis, the “case” of the Ascalaphomerus species is actually a small stick. Instead of assembling a case with silk and pieces of substrate, a larva of this genus gouges the pith from the axis of a single stick (or occasionally some other piece of wood), then transports the hollowed stick or piece of wood as though it were a case constructed of smaller pieces of substrate. The anterior opening of the case is beveled so that if it is in a cathaptotic position, it will be held at an angle to the substrate. During daytime, the substrate is usually a larger, dead tree limb lying on a stream bottom in slowly moving marginal water. When the Ascalaphomerus larva is gripping the dead limb in cathaptosis, its “case” appears to be a broken twig of the tree limb. Larvae of this genus typically remain still and cathaptotic during daylight hours, protected by camouflage from visual hunters. At night they moved more freely, shredding dead plant debris or capturing small animals for food.
In Trichoptera, potential examples of phragmosis (Table
For an animal that lives in a burrow, nest, or portable case or shell, the threshold between their home and the outside world is a transition portal of vital importance. It is the animal’s point of departure from a relatively safe haven to access other vital resources. This vulnerability has served as selective pressure, resulting in the evolution of the defense techniques of phragmosis and cathaptosis. Both techniques seal the opening, but in very different ways.
We have demonstrated the behavioral components of these defensive behaviors for three species and provided lists of some species whose larvae and cases meet their respective, necessary structural criteria. We encourage colleagues to test these hypotheses with the species listed in Tables
Conceptualization: MJB, JCM. Literature review: MJB. Investigation: MJB, LP, H-mZ. Original draft: MJB. Review/editing: MJB, LP, H-mZ, JCM. Supervision: JCM.
The authors declare no conflicts of interest. No other employees of our universities had a role in the design of the study; in the collection, analyses, or interpretation of the data; in the writing of the manuscript; or in the decision to publish the results.
This research was conducted in partial fulfillment of requirements for two Clemson University course sections of Selected Topics in Entomology: “Insect Defenses” and “Biomonitoring with Aquatic Insects” (ENT 4980, sections 1 and 3). The research was accomplished with the facilities of the Clemson University Arthropod Collection and the Department of Entomology, Nanjing Agricultural University. We thank Dr Kenneth Tuite, Department of Languages, Clemson University, for advice about the etymology of cathaptosis. We are grateful for the timely help by Ms Shannon Willis, Director of Digitization at University Libraries, and Ms Kirstin O’Keefev, Clemson University Press, TigerPrints, Clemson University, to post the video results for our study.