View - Kowalewski, M. - Virginia Tech

LABANDEIRA—PREDATORS, PARASITOIDS, AND PARASITESfrom the record of dipteran parasites, particularlythe Culicomorpha, whose adults are free-rangingand not bound to particular host individuals. Withinthe Culicomorpha, the Ceratopogonidae are wellknown to feed on vertebrate blood and hemolymph;this feeding behavior is considered a plesiomorphicfeature within the family (Downes, 1971a; Borkent,1995). The ceratopogonid fossil record extendsback to the Early Cretaceous and, notably, includesseveral extant genera that feed on reptilian blood(Desportes, 1942; Wirth and Hubert, 1989). In lightof this feeding capacity of ceratopogonids, Borkent(1995) examined the correlations between palpaland antennal sensillae, stylet dentition, and whetherthe host organisms were invertebrates, birds, or largetetrapods—the latter determined by downwindplumes of host-generated carbon dioxide and heat(Rowley and Cornford, 1972; McKeever et al., 1991;Blackwell et al., 1992). He concluded that two orthree species of biting midges from Canadian UpperCretaceous amber were parasitizing largevertebrates, most likely co-occurring hadrosaurs (butsee Szadziewski, 1996). Two of the threeceratopogonid genera he identified are extant andsuck blood from large vertebrates, including reptilesand mammals. This plesiomorphic feature of theCeratopogonidae may extend to the rest of thesuperfamily Culicomorpha, appearing in the formof functional piercing mouthparts in females,subsequently lost in lineages such as theChaoboridae (phantom midges), Chironomidae, andDixidae. The Tanyderidae (primitive crane flies), oneof the oldest dipteran lineages, had stylatemouthparts during the Late Triassic and probablyfed on blood (Kalugina, 1991; Borkent, 1995). Basedon this evidence, some authors suggest that stylatemouthparts consisting of a fascicle of 3 to 5 styletsmay be plesiomorphic for the Culicomorpha, witha modest expansion of the labellar pad as a laterdevelopment (Downes and Colless, 1967; Downes,1971b; Fang et al., 1999). According to these authorsit is unlikely that there was repeated evolution ofthe same mouthpart type. However, Pawlowski etal. (1996) provide a molecular phylogenetic analysisindicating at least two independent derivations ofblood feeding within the Culicomorpha; theyconclude that nectarivory is the primitive feedingstrategy. Similarly, Glukhova (1989) proposed thatthe basal Culicomorpha and related taxa initiallywere saprophagous on carrion, and then, throughthe production of salivary proteolytic enzymes, wereable to feed on the external secretions of livingvertebrates, followed by subsistence on blood. Suchan evolutionary shift, however, seems moreappropriate for the origin of advanced blood feedingin (muscoid) flies (Szadziewski, 1996), and certainSoutheast Asian blood-sucking moths (Bänziger,1975). Another hypothesis is that insecthematophagy originated from inquiline associationsin vertebrate nests by a shift from nest detritivoryof epidermis, feces, sebum, and other exudates toblood feeding (Balashov, 1999). This hypothesis ismost relevant to the origin of ectoparasitism in thePhthiraptera, since many members of the closelyrelated Psocoptera are nest associates of vertebratehosts (Waage, 1979).There are two ecologically different approachesto blood feeding. The first is solenophagy—foundin the Culicidae (mosquitoes), Reduviidae (assassinbugs), Cimicidae (bed bugs), and anopluranPhthiraptera (sucking lice)—in which blood vesselssuch as capillaries are punctured with needle-likestylets (Brown, 1989). In contrast, telmophagy—found in the Ceratopogonidae, Tabanidae(horseflies), Muscidae (house flies), and ticks—ischaracterized by the creation of pockets of laceratedtissue that has been slashed by stylets, which inthese organisms are often modified into serratedblades and used in opposition by scissor-likemovements. The insect then drinks the resultingpool of blood and lymph (Brown, 1989). Membersof the Glossinidae (tsetse flies) have uniquepiercing-and-sucking mouthparts and anintermediate strategy for obtaining blood. Althoughglossinid fossils occur in the North American lateEocene (Cockerell, 1917; Grimaldi, 1992),glossinids today are biogeographically restrictedtoday to sub-Saharan Africa. They are currentlymajor vectors for infectious trypanosomiases thataffect ungulates (nagana) and humans (sleepingsickness) (Lehane, 1991). It has been suggested thatnagana-like diseases may have been vectored by235