Strepsiptera

(Strepsipterans)

Class Insecta

Order Strepsiptera

Number of families 9

Evolution and systematics

The Strepsiptera are thought to have originated in the Carboniferous, but the earliest known fossils are from the lower Cretaceous amber of Lebanon. The phylogenetic position of the strepsipterans is unclear, with four possible phylogenetic placements. The first is as the sister group of the beetle family Rhipiphoridae (Coleoptera), which has similar parasitic development, flabellate (branched) antennae, and forewing reduction. The second is as the sister group of beetles (Coleoptera), because they use only the hind wings for flight. The third possible placement is as the sister group of flies (Diptera), which have hind wing halteres (front wing and hind wing halteres could have switched places by a homeotic mutation) and similarities in their DNA. Fourth, they may be placed outside the endopterygote insects, such as beetles and flies, because the pupal stage is preceded by two pharate larval instars (enclosed within the skin of a previous instar), with external wing buds in females, and larval eyes are carried over to the adult stage. The more than 500 described species of strepsipterans are classified in two suborders: Mengenillidia, with two families (one, Mengeidae, known only from fossil males in Eocene Baltic amber), and Stylopidia, with seven families.

Physical characteristics

Strepsipterans have two different morphologies ("hypermetamorphosis"). The first larval instar, called the triungulinid, is free-living and actively host-seeking, and has simple eyes, legs, and two long caudal setae. The second through the last instar larvae (they can have 4 to 7 instars depending on the species) are maggot-like and endoparasitic. Adult males usually are 0.04–0.12 in (1–3 mm) long, with some reaching 0.3 in (7 mm). Females typically are 0.19 in (5 mm) long, but they can range from 0.08 to 1.18 in (2–30 mm). There is extreme sexual dimorphism: adult males look like insects, whereas females look like larvae (larviform) and lack legs, antennae, and external genitalia. Adult males are free living, whereas most females are internal parasites on other insects and remain in the host for their entire lives. Females of the family Mengenillidae are free living.

Males have berry-like eyes, with each lens separated by cuticle or setae; branched antennae; nonfunctional mouthparts; reduced forewings in the form of halteres used for balancing during flight; fan-shaped hind wings with longitudinal veins but no cross veins; and no cerci. Strepsipterans also are called "twisted wing parasites," referring to the peculiar twisted shape of the male hind wings in flight. In the suborder Stylopidia the female head and thorax are united to form a cephalothorax, which protrudes from the body of the host. The female lives within the last larval skin, in which she also pupates, and her whole abdominal cavity is filled with eggs or developing embryos.

Distribution

Although the order is cosmopolitan, most species occur in the tropics.

Habitat

Strepsipterans are found wherever their hosts live. Known hosts include Lepismatidae (Thysanura), Blattidae (Blattodea), Mantidae (Mantodea), Gryllidae, Gryllotalpidae, Tettigoniidae (Orthoptera, Ensifera), Tridactylidae (Orthoptera, Caelifera), Psyllidae (Hemiptera, Sternorrhyncha), Cercopidae, Cicadellidae, Membracidae, Delphacidae, Dictyopharidae, Eurybrachidae, Ricaniidae, Flatidae, Fulgoridae, Issidae, Tettigometridae (Hemiptera, Auchenorrhyncha), Coreidae, Cydnidae, Lygaeidae, Pentatomidae, Scutelleridae (Hemiptera, Heteroptera), Tephritidae, Platysomatidae (Diptera), Formicidae, Vespidae, Sphecidae, Colletidae, Halictidae, and Andrenidae (Hymenoptera).

Behavior

The life cycles of strepsipterans are complex. Eggs are retained within the body of the female until they hatch. The triungulins leave the body of the mother's host and wait for another host. They jump or crawl onto the new host and are transported back to its nest, where they penetrate the host's eggs or developing larvae. The second instar larvae live and feed inside the host's body cavity. Larvae molt four to seven times and reach the last instar at about the same time that the host is ready to pupate. The larvae pupate with their heads and thoraxes protruding between the host's fourth and fifth abdominal segments.

Males use an eversible saclike structure on the head (similar to the ptilinum of some flies) to open the puparium, and leave the host while it is flying; they have only a few hours to find females and mate before dying. Females of the suborder Stylopidia remain in the puparium, protruding from the host for their entire lives, their life spans directly linked to those of their hosts. In the Mengenillidae both sexes abandon the host to pupate externally, and the adults are free living.

Feeding ecology and diet

Parasitic larvae of the second through the last instar and Stylopidia females feed by filtering the host blood; free-living adults do not feed.

Reproductive biology

Female strepsipterans attract males with pheromones. Males fertilize females by injecting sperm into the female's body cavity. Females are sexually mature before molting to the adult stage and give birth to live larvae instead of laying eggs. In some species females are parthenogenetic, reproducing without being fertilized by a male.

Conservation status

No strepsipteran is cited by the IUCN.

Significance to humans

Strepsipterans are not very common, and few people other than entomologists are likely to see them. Although strepsipterans do not kill their hosts, they greatly reduce their nutriment intake; "stylopized" (parasitized by strepsipterans) insects generally are sterile, having been effectively castrated by their parasites. Thus, strepsipterans probably are indirectly beneficial to humans, because they may control population levels of economically important insects. Such insects include Antestia stinkbugs (Hemiptera, Pentatomidae) that attack coffee plantations; fruit flies (Diptera, Tephritidae); long-horned grasshoppers (Orthoptera, Tettigonidae), which defoliate oil palms and coconuts; virus-transmitting leafhoppers (Hemiptera, Cicadellidae), for example, Perkinsiella vitiensis on sugarcane and Nephotettix species on rice; and plant hoppers (Hemiptera, Delphacidae), such as Nilaparvata lugens and Sogatella furcifera on rice.

Species accounts

List of Species

No common name

Halictophagus naulti

family

Halictophagidae

taxonomy

Halictophagus naulti Kathirithamby and Moya-Raygoza, 2000, Tlaltizapán, Morelos, Mexico.

other common names

None known.

physical characteristics

Males have three tarsomeres and seven antennomeres; females are larviform.

distribution

So far known only from its type locality, Tlaltizapán in Morelos, Mexico.

habitat

Parasitizes the corn leafhopper Dalbulus maidis (Hemiptera, Cicadellidae).

behavior

Nothing is known.

feeding ecology and diet

Endoparasitic larval instars and females feed on the body fluids of the host; adult males do not feed.

reproductive biology

Nothing is known.

conservation status

Not listed by the IUCN.

significance to humans

The corn leafhopper Dalbulus maidis is the most important leafhopper pest of maize in Latin America; Halictophagus naulti thus is an important biological control agent.

No common name

Eoxenos laboulbenei

family

Mengenillidae

taxonomy

Eoxenos laboulbenei Peyerimhoff, 1919, Cannes, southern France.

other common names

None known.

physical characteristics

Males have well-developed hind wings and branched antennae with six antennomeres. Females lack wings, but they have eyes, unbranched antennae with four or five antennomeres, and legs. Both sexes leave the host to pupate in the ground.

distribution

Spain, Portugal, southern Italy and southern France, North Africa, and the Canaries.

habitat

Parasitizes several species of silverfish (Thysanura, Lepismatidae).

behavior

Triungulinids (first instar larvae) are very active and jump onto all instars of their host, to penetrate their body cavities. The last larval stage leaves the host and pupates; pupation lasts from one to three weeks. Males usually live only one to two hours.

feeding ecology and diet

Endoparasitic larval instars feed on body fluids of the host; adults do not feed.

reproductive biology

During the summer, larval development takes place quickly. Some females never hatch from the puparium and reproduce parthenogenetically; others hatch and are fertilized by males.

conservation status

Not threatened.

significance to humans

None known.

No common name

Stichotrema dallatorreanum

family

Myrmecolacidae

taxonomy

Stichotrema dallatorreanum Hofenender, 1919, Wogeo, Schouten Islands, Papua, New Guinea

other common names

None known.

physical characteristics

The female is larviform and very large, at about 0.98 in (25 mm), with hooked protuberances.

distribution

Papua New Guinea

habitat

Parasites of the long-horned grasshoppers Sexava nubila, Segestes decoratus, and Segestidea novaeguineae (Orthoptera: Tettigoniidae), which are found on oil palms.

behavior

Male myrmecolacids typically parasitize ants (a pupa of a possible male S. dallatorreanum was found on a Camponotus ant), whereas females utilize grasshoppers, crickets, katydids, or mantids. Triungulinids (first instar larvae) emerge alive from the adult female, which remains endoparasitic in her host. Because the host, with the female, moves around, more triungulinids are dispersed (the host remains alive and acts as the disperser) onto the surface of oil palm leaves. The triungulinids then seek the footpads of passing long-horned grasshoppers, to which they attach to penetrate their new hosts.

feeding ecology and diet

Endoparasitic larval instars and females feed on body fluids of the host.

reproductive biology

On entry into the host, the triungulinid molts into a second instar larva that moves up the host's leg to the abdominal region, where it molts four times but without shedding the old cuticle. Adult females are capable of producing about a million triungulinids. This species is parthenogenetic.

conservation status

Not threatened.

significance to humans

Long-horned grasshoppers defoliate large areas of oil palm plantations in Papua New Guinea; Stichotrema dallatorreanum is released there to help control this pest.

Resources

Books

Carvalho, E. Luna de., and M. Kogan. "Order Strepsiptera." In Immature Insects, Vol. 2, edited by F. W. Stehr. Dubuque, IA: Kendall/Hunt Publishing, 1991.

Kathirithamby, J. "Strepsiptera." In The Insects of Australia: A Textbook for Students and Research Workers, Vol. 2, edited by I.D. Naumann, P. B. Carne, J. F. Lawrence, et al. 2nd edition. Carlton, Australia: Melbourne University Press, 1991.

——. "Strepsiptera of Panama and Mesoamerica." In Insects of Panama and Mesoamerica, edited by D. Quintero and A. Aiello. New York: Oxford University Press, 1992.

Periodicals

Bohart, R. M. "A Revision of the Strepsiptera with Special Reference to the Species of North America." California University Publications in Entomology 7, no. 6 (1941): 91–160.

Kathirithamby, J. "Review of the Order Strepsiptera." Systematic Entomology 14 (1989): 41–92.

Kinzelbach, R. K. "The Systematic Position of the Strepsiptera (Insecta)." American Entomologist 36 (1990): 292–303.

Whiting, M. F. "Phylogenetic Position of the Strepsiptera: Review of Molecular and Morphological Evidence." International Journal of Insect Morphology and Embryology 27 (1998): 53–60.

Other

Pohl, Hans. "Strepsiptera: Twisted-Wing Parasites." 5 Mar. 2002. [7 May 2003] <http://www.strepsiptera.uni-rostock.de/>.

"Strepsiptera: Biology, Genomics, Natural History, and Phylogeny." [7 May 2003] <http://www.strepsiptera.com/>.

Tree of Life Web Project. "Strepsiptera: Twisted-Wing Parasites." [7 May 2003] <http://tolweb.org/tree?group=Strepsiptera&contgroup=Endopterygota>.

Natalia von Ellenrieder, PhD