The historical ecology of aquatic insects: An overview

Palaeogeography, Palaeoclimatology, Palaeoecology, 62 (1988): 477-492

477

Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

THE HISTORICAL ECOLOGY OF AQUATIC INSECTS: AN OVERVIEW R O B I N J. W O O T T O N

Department of Biological Sciences, University of Exeter, Exeter (U.K.) (Accepted for publication April 24, 1986)

Abstract Wootton, R. J., 1988. The historical ecology of aquatic insects: an overview. Palaeogeogr., Palaeoclimatol., Palaeoecol., 62: 477-492. The fossil record of freshwater insects is reviewed. The earliest firm evidence for an aquatic habit in each relevant order is charted, together with the first appearance in time of some important component taxa. The recently expressed view that insects were primitively aquatic and apneustic is briefly discussed. It is neither confirmed nor disproved by the observed distribution of freshwater insects in time. The progressive emergence of insect life-styles in fresh water is discussed and charted. Rheobiontic forms were present in the Lower Permian, but insects may not have played much part in lentic systems before the mid-Triassic. Many early insects were predatory; but benthic periphyton scrapers and fine detritus filterers and deposit feeders may well have been present in running water at an early stage. Pelagic predators and scrapers seem to have been a Mesozoic development; and it may be that cased Trichoptera in the Cretaceous were the first significant insect shredders of coarse plant debris. The radiation of aquatic Diptera, from the Jurassic onwards, was immensely important, revolutionising the structure of many ecosystems and resulting in the colonisation of several new adaptive zones.

Introduction I n s e c t s form so i m p o r t a n t a c o m p o n e n t of m o d e r n f r e s h w a t e r e c o s y s t e m s t h a t it is diffic u l t to e n v i s a g e h o w a n c i e n t s y s t e m s c o u l d h a v e f u n c t i o n e d w i t h o u t them; y e t t h e fossil r e c o r d i n d i c a t e s t h a t t h e c o l o n i z a t i o n by i n s e c t s of t h e b r o a d a d a p t i v e z o n e s w h i c h t h e y now occupy may not have been completed until the Late Cretaceous or early Tertiary. In 1972 I r e v i e w e d w h a t w a s t h e n k n o w n of t h e d i s t r i b u t i o n in t i m e of a q u a t i c i n s e c t groups, and charted the progressive appeara n c e of t h e v a r i o u s l i f e - s t y l e s w h i c h c h a r a c t e r ise m o d e r n forms. T h e p r e s e n t p a p e r is int e n d e d to b r i n g t h a t r e v i e w u p to d a t e . In t h e intervening decade many new faunas have been studied and new insects described, partic0031-0182/88/$03.50

u l a r l y by i n v e s t i g a t o r s in t h e U.S.S.R. T h e q u a n t i t y of t h i s w o r k , a n d i n e v i t a b l e t r a n s l a tion problems, have restricted its a p p r e c i a t i o n o u t s i d e t h e S o v i e t bloc. H o w e v e r , R o h d e n d o r f a n d R a s n i t s y n (1980) p r e s e n t a n i m p o r t a n t a n d useful s u m m a r y in R u s s i a n of t h e r e c e n t v i e w s of t h e M o s c o w s c h o o l on i n s e c t p a l a e o n t o l o g y a n d e v o l u t i o n . S i n c e it r e f e r s to und e s c r i b e d as w e l l as d e s c r i b e d m a t e r i a l , a n d m o r e o v e r i n c l u d e s a c h a p t e r by K a l u g i n a on t h e e v o l u t i o n of i n s e c t s in f r e s h w a t e r , t h i s b o o k h a s p r o v e d a v a l u a b l e s o u r c e of i n f o r m a t i o n for t h e p r e s e n t r e v i e w . T h e field is b r o a d , a n d I h a v e h a d to a c c e p t on t r u s t t h e identific a t i o n of m a n y of t h e i n s e c t s w h i c h h a v e b e e n d e s c r i b e d ; c r i t i c i s m is a m a t t e r for e x p e r t s on each individual group. Useful expert comment, t h o u g h n o t of t h e m o s t r e c e n t w o r k , is to be

© 1988 Elsevier Science Publishers B.V.

478 found in the English edition (1981) of Hennig's

Insect Phylogeny. In addition to newly-described insects and faunas, the last few years have seen the appearance of several theories, using evidence from both fossil and recent forms, which postulate an aquatic or amphibiotic stage in the ancestry of all insects, or at least of all Pterygota (Riek, 1971; Kukalov~-Peck, 1 9 7 8 , 1983; ~tys and Sold~n, 1980). These have profound implications on the evolving roles of insects in fresh water, and it is appropriate that they too should be discussed, The o b s e r v e d d i s t r i b u t i o n o f a q u a t i c i n s e c t s in t i m e The geographic distribution and some of the characteristics of fossil insect-bearing beds, period by period, have been mapped and discussed by Zherikhin (1980), and those of the Palaeozoic by Wootton (1981) who has figured the principal Carboniferous and Permian localities on palaeogeographic maps. To the important Carboniferous sites should now be added Montceau-les-Mines, France, whose rich and promising fauna, Stephanian B in age, is being studied by Burnham (Burnham, 1981). Transference of the insect localities to palaeogeographic maps demonstrates their uneven spatial distribution. With very few exceptions our knowledge of Carboniferous insects is drawn from the coal-bearing belt of Europe and North America, laid down between palaeolatitudes 10°N and 20°S. The Permian beds which have been studied in detail almost all lay between the equator and palaeolatitude 40°N (Belmont, N.S.W., Australia at 60°S is a late Permian exception). Triassic localities are more widespread, between palaeolatitudes 70°N and 70°S; but the enormous majority of known insect-bearing beds from the Jurassic, Cretaceous and Tertiary were laid down in what is now the north temperate zone. While palaeoclimatic changes must be borne in mind, it is broadly true to say that we know comparatively little about non-tropical insect faunas from the Palaeozoic, and of tropical faunas thereafter,

Evidence for the existence of an aquatic group at or by a particular horizon may be of three kinds. (1) Fossils may be found with visible aquatic adaptations, usually relating to locomotion or respiration. This is the strongest kind of evidence, and may be taken as conclusive - provided t h a t the structures are correctly interpreted. (2) Fossils may occur which belong to two or more subdivisions of a single group all of whose present-day representatives are aquatic at some stage of their life-cycle, and assumed to be so by descent from an aquatic common ancestor. Such evidence is less reliable t h a n (1) unless the assumption t h a t the aquatic habit is synapomorphic can be proved. (3) At least one fossil may be found representing a group all of whose extant representatives are aquatic at some stage. This is the least reliable category, as the group may formerly have had terrestrial representatives, but it becomes more reliable the younger the deposit and the lower the taxonomic rank of the group. Since many insect groups are aquatic only as juveniles - - "ontogenetically amphibious" (~tys and Sold~n, 1980) - - and since fossil adults are usually far more commonly found, direct type (1) evidence is often lacking, and one is forced to resort to types (2) and (3). It is the more important to appreciate their limitations. The same categories of evidence can be applied to other aspects of the life-style of insects; for example their food and habitats. In theory a fourth category is also possible, and should be the most precise and reliable of all: direct ecological information (gut contents, burrows etc.) preserved with the insect. In practice such information is rare, and has seldom been used. How these categories of evidence may be applied can be illustrated with reference to the Carboniferous. Until very recently, groups whose later representatives are typically aquatic were known from Carboniferous beds only as adults. These included Triplosoba pulchella Brongniart 1883 (Ephemeroptera)

479 from the Stephanian B of Commentry, France (Carpenter, 1963) and another, undescribed, mayfly from the Stephanian of Montceau-lesMines (Burnham, 1981); and dragonflies of the Order Protodonata (treated by many workers as a suborder of Odonata), including Erasipteron larischi Pruvost 1933 from the Namurian of Czechoslovakia (Kukalov~, 1964), E. bolsoveri Whalley 1979 from the Westphalian A of Britain, and the giant Meganeuridae from the Stephanian. Their presence was type (3) evidence for an aquatic habit, and so inconclusive: it was quite possible, as Kalugina (1980) maintained, that aquatic larvae had not yet evolved in these groups. However, Kukalov~Peck (1983) refers to an undescribed giant mayfly nymph from the Upper Carboniferous of Bohemia, and figures part of a protodonate nymph from the Westphalian C-D of Illinois. She has kindly sent me photographs of these nymphs, each of which bears abdominal structures resembling gills. This is type (1) evidence, provided their interpretation as aquatic respiratory structures is correct. Paradoxically it may now be harder to be sure; if, as Kukalov~Peck claims, abdominal winglets are plesiomorphic for all Pterygota, it may no longer be safe to assume that all the insects bearing them were necessarily using them as gills, Kukalov~-Peck (1983) further refers to large numbers of apterygote Monura, mostly juveniles, in Late Carboniferous deltaic beds in New Mexico, and suggests that, since they are '~too fragile to withstand transport from land by water runoff and streams", they were probably aquatic. Too little taphonomic work has been carried out for this to be conclusive; the possibility of waterside Monura being carried downstream by flooding cannot be ruled out. A variety of unquestionably aquatic insects is present from the Lower Permian onwards, These will be considered group by group. Protodonata and Odonata

The Protodonata (= Superorder Meganisoptera = Infraorder Meganeurina of Order Odonata), which are distinguished from other

odonatoids by their wing venation, are known from the Namurian to the Lias. Their juveniles are almost unknown, and Kalugina (1980) has suggested that they were at most semi-aquatic. The nymph figured by Kukalov~-Peck (1983), however, bears abdominal filaments which have been compared with those of extant euphaeid and polythorid Odonata, and suggest a fully aquatic habit. The Odonata proper (sensu Carpenter, 1960) first appear in the Lower Permian (Artinskian and Kungurian) of the U.S.A. and U.S.S.R., where they are represented by Zygoptera-like species and by small, superficially Anisopteralike forms belonging to the Superorder Protanisoptera. Pritykina (1980), however, suggests that these may be Meganeurina (= Protodonata). Anisozygoptera are first known from the Upper Trias of the U.S.S.R. (Pritykina, 1970) and Australia; and Anisoptera from the Lias of Britain and Germany. The inter-relationships of the subdivisions of Odonata are still controversial, and their interpretation affects the evidence for the age of the aquatic nymphal habit. Fossil nymphs are unknown before the Trias, where they appear at Garazhovka (Ukraine) (Kalugina, 1980). Fraser (1957) regarded Protanisoptera as a blind branch, and derived Anisoptera from Anisozygoptera and the latter from Zygoptera; in which case evidence for an aquatic habit before the first nymphs appear is only of type (3). Carpenter (1931) derived Zygoptera from Lower Permian Protozygoptera, and suggested that Anisozygoptera and Anisoptera might come from Protanisoptera. If this were correct, and if the aquatic habit arose once only, there would be type (2) evidence that dragonfly nymphs were already aquatic in the Artinskian. Pritykina (1980) implies, without detailing her evidence, that the Zygoptera and Anisoptera lineages may have been separate since the Carboniferous. Systematics apart, it appears that forms resembling Zygoptera have been diversifying since the Lower Permian; and that Anisozygoptera were briefly prominent in the Late Triassic, Jurassic and Early Cretaceous, but de-

480 clined with the expansion of the Anisoptera from the Lias onwards. Of extant superfamilies, Calopterygoidea appear first in the Upper Jurassic of Karatau, Kazakhstan (Pritykina, 1968), and a coenagrionoid has now been found in the Wealden (Lower Cretaceous) of Britain (E. Jarzembowski, pers. comm., 1986); but Lestoidea are unknown before the Cenozoic. Aeshnoidea - - a paraphyletic group - - are represented by Liassogomphidae in the Lias, by Gomphidae and Petaluridae in the Upper Jurassic of Europe, and by an undescribed aeshnid in the British Wealden (E. Jarzembowski, pers. comm., 1985). Condalia (Whalley and Jarzembowski, 1985) from the Upper Jurassic of Montsech, Spain, may be an early libelluloid, as Wootton (1972) suggested, or an aberrant gomphid. If the latter is true~ Libelluloidea are unknown before the Upper Cretaceous (Pritykina, 1980). The Aeshnidiidae, from the Upper Jurassic of Europe and the Cretaceous of Australia, and the Hemeroscopidae, which are abundant in the Lower Cretac e o u s b e d s of Mongolia, m a y b e Cordulegastroidea (Fraser, 1957; Pritykina, 1977).

Ephemeroptera The phylogeny of Ephemeroptera has been recently discussed by Edmunds (1972) and by Chernova (1980). Both give dendrograms, which show considerable agreement, though there are differences. Both to some extent review the fossil record, as does Hennig (1981). Kukalovh-Peck's undescribed Carboniferous mayfly nymph has already been mentioned, and may prove to be unequivocally aquatic. In any event, there can be no doubt that mayfly nymphs were in fresh water by the Artinskian. Those described by Kukalov~ (1968) from Oklahoma and Czechoslovakia not only have abdominal gills, but also setose cerci and a caudal filament. One has stout mandibles. All but one were believed by Carpenter (1979) to be Protereismatidae; but more families may be represented (Hubbard and KukalovgL-Peck, 1980). Adult Protereismatidae are also wellknown from Artinskian beds in the U.S.A. and

Czechoslovakia, and the Kungurian of the Urals. A second Lower Permian family, the Misthodotidae (= Eudoteridae, see Carpenter, 1979) is also known from the U.S.A. and the Urals; mainly from adults, which were much smaller than Protereismatidae. Chernova (1965) has described a misthodotid nymph; but its position is perhaps not certain (Carpenter, 1979). In these families, fore- and hind-wings were nearly equal in length; and this may also have been true of Palingeniopsis, from the Kazanian of Russia, and the Mesephemeridae, from the Upper Jurassic of Solnhofen, Bavaria. These, and the curious Xenophlebia (Riek 1976b), from the Upper Trias of South Africa, stand apart from other Mesozoic, Cenozoic and Recent mayflies. So may the Mesoplectopteridae, known as nymphs from the Triassic of France and now the Ukraine (Chernova, 1980), and perhaps as an adult from the Upper Permian of Germany. They are poorly studied, but Chernova (1980) regards them as an offshoot of Protereismatidae. From the Jurassic onwards a variety of mayfly nymphs, subimagos and imagos is known. Their systematic position is controversial, but there is broad agreement that Staeckelbergisca, from the Middle Jurassic of Siberia, has siphlonurid affinities, as probably do a number of other Mesozoic forms (Edmunds, 1972; but note that Siphlonuridae as conceived by Edmunds is entirely paraphyletic, and includes the stems of several other families). Olgisca, from the Upper Jurassic of Bavaria, and Proameletus from the Lower Cretaceous of Siberia, are probably true Siphlonurinae (Sinichenkova, 1976); and Mesoneta from the Upper Lias and Lower Cretaceous of the U.S.S.R., and the Upper Cretaceous Cretoneta Chernova 1971 may be Leptophlebiideae (Chernova, 1971; Hubbard and Savage, 1981). The nymphs Archaeobehningia and Mesogenesia, from the Middle Jurassic of Siberia have been assigned to Behningiidae and Palingeniidae respectively (Chernova, 1977), and those of Mesopalingea (Whalley and Jarzembowski, 1985) from the Upper Jurassic of Spain, have also been placed in Palingeniidae: they are typical bur-

481 rowing types, with large mandibular tusks. Epeoromimus Chernova 1969, was compared by that author with Heptageniidae, by Edmunds (1972) with Siphlonuridae. Heptageniidae are otherwise unknown before the Baltic amber (Eocene) where they appear with Ephemeridae, Ephemerellidae, Baetidae, Metretopodidae and Isonychiidae, and perhaps Potamanthidae and Polymitarcidae. One exclusively Mesozoic family requires mention: the Hexagenitidae, from the Upper Jurassic of Germany and Siberia, and the Lower Cretaceous of Siberia and Mongolia. The spectacular Ephemeropsis, whose wing span reaches 90 mm, and whose nymphs may be 60mm long, is a characteristic component of the widespread lake faunas of the Asian Lower Cretaceous. Demoulin (1971) has suggested that the extant Chromarcys may belong in Hexagenitidae, which may be close to Oligoneuriidae (Edmunds, 1972).

Aquatic "Protorthoptera" The affinities of the many Palaeozoic Protorthoptera (sensu Carpenter, 1966 and elsewhere) are slowly becoming clearer, but their life-histories are still poorly known. Some nymphs have serial abdominal gill-like appendages, and may have been aquatic. Some at least belong to the Family Lemmatophoridae, which occurs in Lower Permian beds in the U.S.A., the Urals and Czechoslovakia. The best-known nymphs are from the Artinskian of Kansas (Carpenter, 1935; Kukalov~-Peck, 1978). Riek (1976a) has described a nymph with gills - - apparently not a lemmatophorid - - from the Lower Permian of South Africa. Protorthoptera are rarer in the Upper Permian, where they are progressively outnumbered by Plecoptera (Kalugina, 1980).

Plecoptera Zwick (1973; and in Hennig, 1981) has published a phylogenetic classification of Plecoptera; and he and Hennig (1981) discuss the fossil record, as does Rasnitsyn (1980).

Stoneflies first appear in the Lower Permian (Kungurian) of the Urals and the Vorkuta Basin, U.S.S.R., and are also known from the Upper Permian of Siberia, the Urals and Kazakhstan, the Upper Permian and Upper Triassic of South Africa and Australia, and the Upper Triassic of Argentina. The allocation of these early forms is controversial. Illies (1965), Riek (1973, 1976c, d), Pinto and Purper (1978) and other authors have referred several to modern families, including Eustheniidae, Gripopterygiidae and Taeniopterygiidae. Zwick (1979)described the placing in the Eustheniidae of Stenoperlidium, from the Upper Permian and Upper Trias of Australia, as probable but unproven, and (in Hennig, 1981) has stressed that the alleged affinities of all the Permian and Mesozoic forms are based on plesiomorphic characteristics, and hence unreliable. For the same reason, he does not accept the assignment of Mesozoic species to Leuctridae, Taeniopterygidae and Perlidae, though he suggests that Mesoleuctra and Mesonemoura from the Jurassic of the U.S.S.R., and Sinonemoura, from the Cretaceous of China, could be Nemouroidea. Many of the known Palaeozoic and Mesozoic Plecoptera are nymphs, but few show clear aquatic adaptations. Although they may well have been in water from the first, the earliest specimen providing type (1) evidence of this may be an Upper Permian nymph of Stenoperlidium from Australia which shows the bases of fingerlike abdominal gills (Tillyard, 1935). Early Cenozoic stonefly juveniles are almost unknown, but the Eocene Baltic amber contains many adults, and provides reliable first records of several extant Holarctic families, including Perlodidae, Perlidae, Leuctridae, Nemouridae and Taeniopterygidae. Zwick (in Hennig, 1981) suggests that the Eocene Holarctic fauna was similar at the family level to that of today.

Aquatic Heteroptera The fossil and Recent Nepomorpha (= Hydrocorisae) have been monographed by

482 Popov (1971), and he has since (Popov, 1980) reviewed the fossil Hemiptera as a whole, plotting the distribution of the groups in time on a phylogenetic tree. The earliest recorded waterbugs have been found in early Upper Triassic (Carnian) lacustrine beds in North Carolina and Virginia (U.S.A.) (Olsen et al., 1978). They have been figured, but not described, and their affinities are uncertain. Naucoroidea are known from the topmost Trias of the Ukraine and Soviet Central Asia (Popov, 1980), and from the Lias and Middle and Upper Jurassic of Central Asia and of Germany; Corixoidea from the Lias and Middle and Upper Jurassic of Soviet Central Asia and the Lias of Siberia; and Notonectidae from the Lias of Central Asia. Belostomatidae are now known in the Lower Lias of England (Whalley, 1985); and the Nepoidea are otherwise spectacularly represented in the Upper Jurassic of Solnhofen, Germany, by Laccotrephes (Nepidae), Mesonepa and Mesobelostomum (Belostomatidae), and the curious Stygeonepa, with oar-like metathoracic legs. The first representative of Gerromorpha (=Amphibicorisae) may be Engynabis tenuis Bode 1953, from the Upper Lias of N.W. Germany (Popov and Wootton, 1977). In the Upper Jurassic the Karanabidae from Kazakhstan and the giant Chresmoda from Solnhofen may well be Gerromorpha (Popov, 1980), though the latter has previously been supposed to be a phasmid; and Baudoin (1980) has calculated that it was too large to have been supported by the surface film. Extant gerroid families are unknown before the Tertiary. Andersen (1982) suggests that gerroids have colonised the surface film independently several times.

Megaloptera Permosialis Martynov, from the Upper Permian of the U.S.S.R., is now regarded as a member of Miomoptera (Riek, 1976d; Rasnitsyn, 1977); but Ponomarenko (1977a) has described new megalopteran wings from the Upper Permian of European Russia, placing them in the

new Family Parasialidae, which he regards as the sister-groupoftheSialidae. He also transfers to Megaloptera Tychtodelopterum, from the Upper Permian of Siberia. The Upper Permian larva described from European Russia by Sharov (1953)is no longer likely to be that of Permosialis, and Ponomarenko (1977a) refers it to Parasialidae; but Riek (1976d) suggests that it is a corydaloid. In either case, and if it is assumed that the abdominal appendages functioned as gills, it provides type (1) evidence for an aquatic habit. However Achtelig (in Hennig, 1981) points out that its small head and prothorax are more reminiscent of a gyrinid-like beetle larva than a megalopteran. Mormolucoides Hitchcock 1858, from the Trias of the U.S.A., may be megalopteran larvae. Euchauliodes, from the Upper Triassic of South Africa, may be an early corydaloid side-branch (Riek, 1974). Cretochaulus, known as wings and nymphs from Lower Cretaceous deposits in Siberia, is thought to be a chauliodine corydalid, and Chaulosialis, from Upper Cretaceous amber of the Taimir Peninsula, is perhaps a young sialid larva (Ponomarenko, 1976).

Aquatic Coleoptera Kalugina (1980) refers to aquatic "Schizocoleidae" in Upper Permian beds, and the possibility that the Upper Permian alleged megalopteran larva may be a beetle is referred to above. Some Triassic Schizophoridae (Ponomarenko, 1969) and Triaplidae (Ponomarenko, 1977b) may have been aquatic (Kalugina, 1980). But the first clear type (1) evidence of swimming adults seems to be Jurassic, where various Hydradephaga occur: Liadytidae in the Lias of Siberia (Ponomarenko, 1963), and in the Upper Jurassic, Coptoclavidae from Siberia and Kazakhstan, Parahygrobiidae from Siberia and Bavaria (Ponomarenko, 1977b), and Gyrinidae from Kazakhstan (Ponomarenko, 1973). The first water beetle larvae are also Jurassic: Angaragabus, from the Lias of Siberia (Ponomarenko, 1963), and Parahygrobiidae and Coptoclavidae (Ponomarenko, 1977b).

483

Some spectacular Lower Cretaceous Hydradephaga are known. Coptoclava longipoda, a prominent member of many Cretaceous Asian lake faunas, has been described in detail by Ponomarenko (1975). Both larvae and adults had raptorial prothoracic, and flattened mesoand metathoracic limbs. Dytiscidae, and further Liadytidae and Gyrinidae have been found in Soviet Asia (Ponomarenko, 1977b). Apparently aquatic Hydrophilidae occur for the first time in the Lower Cretaceous of Siberia (Ponomarenko, 1977b).

Trichoptera Sukacheva (1980) reviews the occurrence in time of fossil trichopterous families, and gives a phylogenetic tree. She recognises the Protomeropidae, from the Lower Permian of Kansas and the Upper Permian of Australia; and the Microptysmatidae, from the Lower and Upper Permian of the U.S.S.R., as the earliest Trichoptera. These, and the Upper Permian and Lower Triassic Cladochoristidae from Australia and Soviet Central Asia, the Upper Triassic Prorhyacophilidae from Australia and Soviet Central Asia, and the well-known Necrotauliidae from the Upper Triassic, Jurassic and Cretaceous of Europe and Asia, are probably known only as adults, and almost exclusively as wings. This presents a taxonomic and palaeontological dilemma. Ross (1967), Hennig (1981) and Kristensen (1981) have stressed that one cannot distinguish on grounds of venation alone between the primitive members of Trichoptera (now almost all with aquatic larvae) and Lepidoptera (now almost exclusively terrestrial). The two groups may well have separated no earlier than the Jurassic, so that all earlier "Trichoptera" may represent the common stem group of the two orders; and there is no reason to suppose that their larvae were aquatic. The first larvae, and hence the earliest type (1) evidence for an aquatic habit, are from the topmost Jurassic (Sukacheva, 1982); but Sukacheva (1973) believes that Prophilopotamus asiaticus, from the Middle Trias of Soviet

Central Asia, is a true philopotamid. If, as she supposes, the Triassic Prorhyacophilidae are ancestral to extant Rhyacophilidae, this is type (2) evidence for an aquatic larval habit in the Middle Trias, and this is further supported by the presence of other extinct families apparently of both Annulipalpia and Integripalpia in the Jurassic. Sukacheva (1980, 1982) recognises the Baissoferidae, from the Upper Jurassic and Lower Cretaceous of Asia, as a possible stem group for the Integripalpia. According to her, Rhyacophilidae are represented in the Upper Jurassic; Phryganeidae in the Lower Cretaceous with Baissophryganoides, from Siberia; Rhyacophilidae, Hydroptiliidae, Sericostomatidae, and Leptoceridae in the Upper Cretaceous; and most other modern families by the Oligocene. Trichopterous larvae are known almost exclusively from their cases; and Sukacheva (1982) reviews and gives keys to a number of species, some new, some previously described, from Cretaceous and Tertiary deposits. It is evident that caddises were in the Lower Cretaceous already capable of constructing complex cases from a variety of materials: sand, small stones, the shells of Ostracoda, Conchostraca, gastropod and bivalve molluscs, and various kinds of plant debris.

Aquatic Diptera Rohdendorf (1964, 1980) and Hennig (1981) review the fossil Diptera. These first appear in the Triassic; but the larvae and larval habit of Triassic and many Jurassic Diptera are quite unknown. Most Jurassic forms are Tipulomorpha, and it is quite possible that some had aquatic or semiaquatic larvae; but the first type (1) evidence consists of larval and pupal Chaoboridae, of the Subfamily Chironomapterinae, from the Lower or Middle Jurassic of Siberia (Kalugina, 1977). Larval, pupal and adult Chironomidae, Subfamily Podonominae, occur in Middle to Upper Jurassic beds in Siberia (Kalugina, 1980). Adult Chironomidae, allegedly Tanypodinae; and tipulid pupae, perhaps Limoniinae, are known from the

484 Upper Jurassic of Soviet Central Asia (Kalugina, 1980). Pupal and adult Chaoboridae are fairly frequent in the Coptoclava/Ephemeropsis faunistic complexes of the Asian Lower Cretaceous lakes, and Limoniinae are also present (Kalugina, 1980). Lebanese amber, dated as Neocomian to Aptian, contains Orthocladiinae and Tanypodinae, Ceratopogonidae, and a phlebotomine psychodid (P. E. S. Whalley, pers. comm., 1985). Kalugina (1974, 1976) has described diamesiine and aphroteniine Chironomidae, along with Orthocladiinae, Tanypodinae and Podonominae in Upper Cretaceous (Coniacian-Lower Santonian) amber from N. Siberia. She also records a single chironomine; but stresses (Kalugina, 1980) that members of this subfamily, so prominent today, are very rare before the mid-Cenozoic. Chaoboridae are rarer in the Cenozoic than in the Mesozoic. Of other families, Stratiomyiidae, Dolichopodidae and Empididae are recorded from Upper Cretaceous amber of Canada (McAlpine and Martin, 1969), and Simuliidae may be present in the Cretaceous (Rohdendorf, 1980), but Tabanidae and Culicidae are unknown before the Eocene (Green River and Baltic amber respectively), Discussion

Fresh water in the early evolution of insects The orthodox view that all aquatic insects are secondarily derived from fully terrestrial forms with open tracheal systems has recently come under attack, ~tys and Sold~n (1980), in a valuable study of persistent tracheal gills in adult insects, evaluate this theory alongside three others, due to Riek (1971), to Kukalov~-Peck (1978) and to themselves, which include an aquatic stage in the evolutionary history of all Pterygota. More recently Kukalov~-Peck (1983) has proposed a new theory, which combines aspects of her earlier model with that of ~tys and Sold~n. Following these authors, she proposes that the tracheal system evolved in the aquatic common ancestors of myriapods and insects,

and was initially closed, with " p r e s p i r a c l e s " - whose rSle was wholly developmental - - linking the tracheae with the external cuticle. Spiracles evolved once only, in later myriapod/ insect ancestors which are assumed to have had aquatic early instars and amphibiotic ( = " e u a m p h i b i o u s " ) later instars. Thereafter, fully terrestrial myriapod, apterygote and pterygote groups arose from time to time from stocks which themselves retained the primitive "ontogenetically amphibious" (sensu ~tys and Sold~n) life-history and the primitive closed tracheal system in the juveniles. Several terrestrial groups secondarily developed aquatic representatives, some of which continued to breathe air through open spiracles, others becoming secondarily apneustic. Wings evolved in the later instars of early ontogenetically amphibious insects, from movable '~winglets"; a series of which, on all the trunk segments, had arisen long before in the early apneustic tracheate stock. The contrast between this and the orthodox theory has profound implications on the evolving roles of freshwater insects. If the orthodox story is correct, all aquatic insects are secondarily so. We might then expect to find that early freshwater ecosystems had no insects, and that aquatic groups with terrestrial precursors appear progressively through time. If, however, the aquatic or the ontogenetically amphibious state is primitive for Pterygota or for insects as a whole, then these have been a component of freshwater systems since the Silurian or the Devonian; and several major groups have been aquatic from the first. If Kukalov~-Peck (1983) is correct, Odonata, Ephemeroptera, Plecoptera, Megaloptera, Trichoptera, and perhaps sisyrid Neuroptera and gyrinid Coleoptera are products of a prolonged, unbroken radiation of ontogenetically amphibious types from which all fully terrestrial insects have arisen; and the aquatic habit is therefore secondary only among Heteroptera, Diptera, and other Neuroptera and Coleoptera. Kukalov~-Peck (1978, 1983) has presented palaeontological and neontological evidence in support of her view. Much of this relates to

485

the origin of wings, and the significance and homology of the abdominal "winglets" which she believes to be part of the ground-plan of all pterygote insects; to be serially homologous with wings; and sometimes to have functioned in aquatic respiration, as they do - - usually in a modified form - - in many extant aquatic juveniles. One might hope to find in the fossil record further information which would help in evaluating the opposing theories: for example evidence of aquatic forms linking known aquatic orders, or alternatively ancestors and sister-groups of aquatic types, which themselves appear to have been terrestrial, or less fully adapted to life in water. Unfortunately this is not yet so. We have no direct information on the habits of the common ancestors of the extant ontogenetically amphibious orders; and we know terrestrial precursors and sistergroups only among Hemiptera, Coleoptera and Diptera, in which the aquatic habit is generally agreed to be secondary. The observed distribution of aquatic insects in time is therefore compatible with either theory. Kalugina (1980) suggests that there were no aquatic insects in the Carboniferous; but this is based on the very limited range of habitats from which insects are known, and now appears not to be so. The presence - - but scarcity - - of Ephemeroptera suggests that they were not typical inhabitants of the coalswamps, lowland lakes and deltas on which our knowledge of Carboniferous insects is founded; and the almost complete absence of aquatic mayfly nymphs from these habitats does not preclude their existing in numbers elsewhere particularly in running waters, whose higher oxygen content might be expected to favour apneustic forms. The fact t h a t the first aquatic groups to appear as fossils characteristically today have apneustic juveniles lends support to the theory that apneusty is the primary condition. On the other hand it should be realised t h a t most airbreathing insects can stand temporary immersion; and t h a t the further development of this ability into active life underwater, breathing -

-

air via a physical gill, could have been achieved in relatively generalised insects by means of simple adaptations - - like hydrofuge hairs - - which would be unlikely to show in fossils. Air-breathing aquatic larvae - - which could include the ancestors of apneustic types - - m i g h t easily pass unrecognised.

The progressive colonisation of adaptive zones In 1972, on the evidence then available, I drew the following provisional conclusions (Wootton, 1972). (1) Most early aquatic insects were rheobiontic; and many major aquatic groups began in running water and only later moved into lentic habitats. (2) Most early aquatic insects were at least partly predaceous; and a predaceous habit was primitive for many important groups. How far do these generalisations still seem true? Figure 1 shows the first reasonably reliable records of a number of important extant groups at various taxonomic levels between order and subfamily. The earliest type (1) evidence of aquatic habit is shown for each order, together with the first evidence of type (2) where this predates that of type (1). Wholly extinct groups are not shown, and it must be borne in mind that their ways of life are usually unknown. The generalisation that most Permian and Triassic aquatic insects were rheobiontic still seems plausible. Lower Permian juveniles are rare - - those of Odonata and Trichoptera are unknown - - and it seems unlikely that they were present in any numbers in the places where fossilisation was occurring. The nymphal Lemmatophoridae (Protorthoptera) from Kansas may be an exception; but the mayfly nymphs of Oklahoma and Moravia are thought to have been washed in by streams (Carpenter, 1947; Kukalov~, 1963, 1968). Furthermore most extant Plecoptera are rheobiontic, as are Megaloptera and primitive Annulipalpia and Integripalpia (Trichoptera); and it seems probable that this was true of their Permian and Triassic representatives.

486

U. CARB.

PERMIAN

TRIASSIC

JURASSIC

CRETACEOUS

TERTIARY

ODONATOIDEA

i

Aeshnoidea Libelluloidea v Calopterygoidea Coenagrionoidea 1

t;

,7

EPHEMEROPTERA

v

keptophlebiidae ~iphlonuridae

Saet~ae Ephemerellidae v Hept~geniidae Ephevmeridae

Palinge niidae Bvehningiidae 1

PLECOPTERA

Antarctoperlaria Vl

1

Gripopter ygidae

Perlodidae Perli~ae v Leuctridae Capmidae ? Taen~)pterygidae

Nemouridae

AQUATIC HETERI)PTERA

Navucoroidea Nvepoidea Notonectoidea rixoidea Gerroidea 1 MEGALOPTERA = = = i.~-.C or ydaloidea 1

Sia/oidea

AQUATIC COLEOPTERA

Hydradephaga Gyrinidae 2.====== T R I C H O======= PTERA ?P;hilopot amidae

Dytiscidae HydroPvhilidae

Rhyacophilidae v

Psychomyiidae v

Hydropsychidae v

Phryganeidae Hydroptilidae Polycentropodidae v v . LevptocerJdae Stenopsychidae Serico~ornatidae Gtossosornatidae

Helicopsychidae VGoeridae v

Brachycentridae Beraeidae

Odontoceridae Molannidae v Lepidostomatidae

Lim%ephilidae 1 =

DIPTERA

==El

Chaoboridae ?Podovnom~nae

Tagypodinae Limoniinae

Or t hocladiinae v

Aphvroteniinae

Diarnesiinae Ch~onominae Ceratopogonidae v Phlebotominae

Empi~idae Stratiomyidae DoI~chopodidae

Ta~anidae Culicidae v

Fig.1. The distribution in time of extant insect orders; and the first records of selected extant component taxa. The numeral 1 shows the first type (1) evidence for an aquatic habit; 2 shows the first type (2) evidence, where this precedes type (1). The broken lines indicate the time-span within which the order, or the aquatic habit within it, probably arose.

487 Not until the Late Triassic and Early Jurassic do we have hard evidence of an abundant still-water fauna, with the rapid diversification of water beetles, water bugs and early aquatic Diptera. The Ephemeroptera too seem to have extended their habitat-range: the Liassic Epeoromimus and the Upper Jurassic and Cretaceous Ephemeropsis are thought on morphological grounds to have had swimming nymphs inhabiting still water (Chernova, 1961, 1970). In the Jurassic and Cretaceous a r e m ar ka bl y large number of extant families and even subfamilies appear; and it is probably reasonable to assume th at there was an insect component in the faunas of most kinds of Cretaceous freshwater ecosystem. Recent studies on the communities of the Lower Cretaceous lake systems of Mongolia and Siberia (Zherikhin, 1978; P o n o m a r e n k o and Kalugina, 1980; Ponomarenko, 1983) have demonstrated the existence of several distinct faunistic complexes, presumably characterising different types of

U. CARB.

PERMIAN

TRIASSIC

lentic habi t at over a wide geographical area. By the Eocene the modern aquatic insect fauna seems to have been largely established, at least at the level of family; sometimes of subfamily and even genus. It seems probable t hat many species were occupying both habitats and niches which were broadly similar to those of their extant relatives. The developing pat t ern of food exploitation can also to some extent be traced t h r o u g h time, though the process involves some guesswork about the diets of extinct groups. Figure 2 plots the first clear fossil evidence of particular feeding strategies, and indicates the time-range within which the strategies probably arose. The preval ence of the p r e d a t o r y habit among early forms is still apparent. O donat a and M e g a l o p t e r a were presumably always predatory. The large p r o g n a t h o u s mandibles of one of the Lower P e r m i a n prot erei sm at i d mayfly nymphs (Kukalovfi, 1968) suggest t hat they too were predators. In the Jurassic the

JURASSIC

CRETACEOUS

TERTIARY

Surface-film predation

Pelagic predation

_

_

_.#

. . . . . . .

Pelagic filtering

.~.

Pelagic periphyton-scraping

-# Benthic predation

Benthic coarse debris-shredding

Benthic net-filtering

-#

Benthic periphyton-scraping

Benthic deposit-feeding

.#

..... Burrowing alga and detritus-feeding

---°1

Benthic direct filtering

¢r 1

Burrowing net-filtering

Fig.2. The origins of insect feeding strategies. The star shows the earliest fossil evidencefor a strategy; the broken lines the time within which the latter probably arose. Note that the evidence is often only of type (3); but it is generally probable that the strategy arose earlier rather than later.

488 diversification of naucoroid and nepoid Heteroptera, of dytiscoid beetles and chaoborid flies marks the development of predation in midwater forms, and the presence of Notonectoidea, Gerroidea and Gyrinoidea indicates that surface-film predation was underway. What is less clear is how far Permian and Mesozoic insects were exploiting other food sources. In considering this, it is important to consider what was available, and what other animals may have been competing with insects for available resources, Aquatic macrophytes are unknown before the Trias; but these may be the only major category of primary production which was missing from Palaeozoic systems. There seems no reason to doubt that phytoplankton, aufwuchs (microscopic plants and bacteria on submerged surfaces), filamentous algae and Charophyta, and allochthonous input from waterside vascular plants all contributed to Carboniferous and Permian food webs, as they do today. The relative importance of these components would have varied from habitat to habitat both globally and locally; but all would somewhere have been available for insects to exploit, if they were capable of doing so. In running water, where allochthonous input is particularly important, the amount of waterside vegetation would have been crucial; and the colonisation of streams by insects may have been delayed until an upland flora was established. From that point the possibility of detritus-filtering was open; and it may well be that early Annulipalpia (Trichoptera) had already adopted this way of life in the Trias, or even earlier, even though the allocation of the Middle Triassic Prophilopotamus to the modern drift-filtering family Philopotamidae may not be entirely justified, While we have no proof, it is probable that stone-encrusting algae and bacteria were established early in running water. These provide food today for a variety of scraping insects, mainly Ephemeroptera (Heptageniidae, Baetidae, Ephemerellidae), Plecoptera (relatively few), Coleoptera (Elmidae), Trichoptera (Glossosomatidae, Odontoceridae,

Helicopsychidae, some Limnephilidae and Leptoceridae), and Diptera (some Chironomidae) (Cummins, 1973; Hynes, 1976; Mackay and Wiggins, 1979; Brittain, 1982; Oliver, 1971). None of these families is known before the Jurassic, and most first appear in the Tertiary, but it is entirely possible that some of the Upper Permian, Triassic and Jurassic mayflies, stoneflies and caddises were feeding in this way. The majority of extant Ephemeroptera feed on deposited fine detritus (Brittain, 1982); and this is true of some members of the archaic Siphlonuridae and of the Leptophlebiidae, both of which families are reliably recorded in the Jurassic. Again there is no reason to d o u b t - but also no direct evidence - - that some earlier mayflies were feeding similarly. So probably were some stoneflies: plant debris, coarse and fine, is again the principal food of most modern families (Hynes, 1976). It is quite possible, therefore, that insects in Triassic or even in Permian rivers were exploiting most of the broad categories of food which they do today, even though some important modern groups were wholly absent. The presence in the Jurassic of palingeniid and behningiid Ephemeroptera indicates the arrival of burrowing detritus feeders. Both families today bury themselves in silt, and are thought to feed directly on buried organic material. The most significant new development in running water, however was the appearance in the Jurassic of aquatic Diptera, of whose spectacular expansion and diversification in the later Mesozoic and early Tertiary we are now becoming aware. Brundin (1966) believed that Chironomidae arose in fast montane streams, and only later colonised slow and still waters. Podonominae and Diamesiinae, first known respectively from the Middle Jurassic and the Upper Cretaceous, are today primarily rheophilic, as are many Orthocladiinae, which are present in the Lower Cretaceous. All three subfamilies are predominantly alga and diatom feeders (Oliver, 1971). They, and the Simuliidae, which may have arisen in the Cretaceous and which added to the drift-filtering communi-

489

ties of fast waters, must in addition have provided a rich food source for predatory insects, particularly Plecoptera, Trichoptera and Odonata, as well as for fish. The colonisation of adaptive zones in still water seems to have happened more slowly. Here phytoplankton would from the start have been the principal source of primary production. Ostracoda, very numerous in many Upper Palaeozoic freshwater deposits, seem to have been the principal grazers, and Conchostraca and bivalve and gastropod molluscs dealt with the detritus, in company perhaps with annelids unknown to us. In some brackish and freshwater Carboniferous and Permian communities pygocephalomorph and syncarid Crustacea may have acted as scavengers and low-level carnivores (Schram, 1981). Eurypterida, fish, and aquatic Amphibia and reptiles would variously have occupied the higher trophic levels. The Lower Permian lemmatophorid nymphs may indicate an insect component in some still-water communities; but the first real evidence of a significant insect presence may be the numerous and as yet unstudied water bugs in the early Upper Triassic lake beds of North Carolina and Virginia, heralding the spectacular radiation of Hydrocorisae in the Late Trias and Jurassic, alongside diving beetles and chaoborid flies, Further information can be expected from Triassic beds in the Vosges and the Ukraine, when these have been investigated in detail, Both faunas contain lentic mayflies (Family Mesoplectopteridae), and the Ukraine locality has produced the earliest dragonfly n y m p h - - a zygopteran (Kalugina, 1980). The majority of these insects were certainly predators; the dragonfly benthic, the Hydrocorisae and Hydradephaga variously benthic and mid-water; although the distinction would be artificial if, as seems probable, there was already in the Upper Trias a significant growth of macrophytes. The presence of corixoid Heteroptera in the Lower Jurassic is interesting. Today these insects are specialist feeders on epiphytic plants, a way of life which has required substantial mouthpart modifications,

While it is not certain that the Jurassic forms had already adopted this life-style, the possibility is there. The food of Mesoplectopteridae is unknown; but their presence in the Trias, and that of other presumed still-water mayflies (Staeckelbergisca,Epeoromimus in the Jurassic, and the Hexagenitidae in the Jurassic and Lower Cretaceous) indicates that Mesozoic Ephemeroptera played a significant part in limnic systems then, as they do today. A major event at the Jurassic-Cretaceous boundary is the appearance of cased Trichoptera larvae, which are numerous in the Lower Cretaceous of Mongolia and Siberia, The diet of cased caddises today is very varied - - they include predators, scrapers, diatom filterers and grazers of living plants - - and their habitats range from streams to marshes; but it seems probable that many Cretaceous forms, like very many modern forms, were shredders of coarse plant material. Their arrival indicates an expanding role for insects in the processing of coarse material in still water. It is impossible with any certainty to assign the Mesozoic cases to families. Adult Limnephilidae, perhaps the most important family of shredders today, were present in the Eocene (Wilson, 1978). Two broad feeding strategies remain; and these may indeed have been the last to be adopted by insects in fresh water. Today the characteristic insect group of lake bottoms, fine river sediments and similar situations is the Subfamily Chironominae of the Chironomidae. With some exceptions, these live in tubes, in or on the substrate, feeding on fine detritus either directly or by net-filtering (Walshe, 1951). There is one Upper Cretaceous record, but it seems clear that the subfamily did not begin to approach its present importance until the Late Eocene; and we know of no other insect group which preceded the Chironominae in this adaptive area. In the Eocene, too, are the first records of Culicidae, today the only insect group seriously to compete with the crustacean zooplankton in filtering phytoplankton and fine suspended detritus at the surface of still waters.

490 Conclusion F r e s h w a t e r e c o l o g y is a complex discipline, O u r k n o w l e d g e of the f u n c t i o n i n g even of familiar m o d e r n e c o s y s t e m s is still incomplete, a n d m a n y o t h e r s - - less accessible - - are a l m o s t unstudied. To g e n e r a l i s e a b o u t systems in the r e m o t e past will seem a b s u r d l y speculative a n d simplistic to most n e o e c o l o g i s t s - - a n d

with some justification. The p r e s e n t r e v i e w c e r t a i n l y oversimplifies; just h o w far will be a p p a r e n t only as investigation proceeds. A t all periods since fresh w a t e r was colonised, a q u a t i c e c o s y s t e m s m u s t h a v e been diverse; and o u r k n o w l e d g e of t h e i r insect f a u n a s at all h o r i z o n s is based on u n b a l a n c e d and e r r a t i c samples. We k n o w the P a l a e o z o i c s i t u a t i o n m a i n l y from t r o p i c a l c o a s t a l lakes, deltas and pools, with i n p u t from s t r e a m s and rivers; the Trias from similar b u t m o r e temperate h a b i t a t s in b o t h hemispheres; the J u r a s s i c from fluviatile deposits a n d a few significant lakes and l a g o o n s in t e m p e r a t e E u r a s i a , and the C r e t a c e o u s from a m b e r and a wider r a n g e of lakes, m o s t l y o l i g o t r o p h i c a n d a l m o s t all H o l a r c t i c . I n the v a r i e d h a b i t a t s of the Tertia r y and Q u a t e r n a r y we find f a u n a s with a d i s t i n c t l y m o d e r n a p p e a r a n c e , at least with respect to t h e i r c o n s t i t u e n t families and subfamilies; and the signs are t h a t all the m a j o r a d a p t i v e zones h a d been colonised by the end of the Eocene. As the range of investigated habitats extends, so will o u r k n o w l e d g e of the time-ranges of the insect g r o u p s a n d of t h e i r feeding strategies; and we m a y hope in time to v i n d i c a t e or disprove a q u a t i c theories of the origin of insects, a n d to gain a far c l e a r e r p i c t u r e of t h e i r e v o l u t i o n in fresh water. I suspect, t h o u g h , t h a t several l a n d m a r k s , app a r e n t now, will still be e v i d e n t as w o r k proceeds. These are: the i n c r e a s e d role of insects in still w a t e r s with the a r r i v a l of a q u a t i c m a c r o p h y t e s a n d of a i r - b r e a t h i n g Hete r o p t e r a a n d C o l e o p t e r a in the e a r l y Mesozoic; the d e v e l o p m e n t of a m a j o r s h r e d d i n g i n d u s t r y a m o n g the T r i c h o p t e r a of the L a t e J u r a s s i c and C r e t a c e o u s , c o i n c i d e n t with the rise of the

angiosperms; and a n e n o r m o u s e x p a n s i o n r e a s s o r t m e n t of the roles of insects in f r e s h w a t e r h a b i t a t s as a result of diversification of a q u a t i c D i p t e r a from L a t e J u r a s s i c t h r o u g h the Tertiary.

and all the the

References Andersen, N. M., 1982. The Semiaquatic Bugs (Hemiptera, Gerromorpha). Phylogeny, Adaptations, Biogeography and Classification. Entomonograph 3. Scandinavian Science Press, Malov, Denmark, 454 pp. Baudoin,R., 1980. Sur les Gerris des miroirs d'eau actuels et les Chresmoda des lagunes post-recifales portlandiennes de Solnhofen. Ann. Sci. Nat. Zool. Paris, 2: 111-116. Brittain, J. E., 1982. Biology of mayflies. Annu. Rev. Entomol.,27: 119-147. Brundin, L., 1966. Transantarctic relationships and their significance as evidenced by chironomid midges, with a monograph of the Subfamilies Podonominae and Aphroteniinae, and the austral Heptagyiae. K. Sven. Vetensk. Akad. Handl., 11: 1-472. Burnham, L., 1981. Fossil insects from Montceau-les-Mines (France). A preliminary report. Bull. Soc. Hist. Nat. Autun, 100: 5-12. Carpenter, F. M., 1931. The Lower Permian insects of Kansas. Part 2. The Orders Palaeodictyoptera, Protodonata and Odonata. Am. J. Sci., 21: 97-139. Carpenter, F. M., 1935. The Lower Permian insects of Kansas. Part 7. The Order Protoperlaria. Proc. Am. Acad. Arts Sci,, 70(4): 103-146. Carpenter, F. M., 1947. Lower Permian insects from Oklahoma. Part 1. Introduction and the Orders Megasecoptera, Protodonata and Odonata. Proc. Am. Acad. Arts Sci., 76(2): 25-54. Carpenter, F. M., 1960. Studies on North American Carboniferous insects. 1. The Protodonata. Psyche, 67(4): 98-110. Carpenter, F. M., 1963. Studies on Carboniferous insects of Commentry,France. Part 4. The genus Triplosoba. Psyche, 70(2): 120-128. Carpenter, F. M., 1966. The Lower Permian insects of Kansas. Part 11. The Orders Protorthoptera and Orthoptera. Psyche, 73(1): 46-88. Carpenter, F. M., 1979. Lower Permian insects from Oklahoma. Part 2. Orders Ephemeroptera and Palaeodictyoptera. Psyche, 86(2-3): 261-290. Chernova, O. A., 1961. The systematic position and geological age of mayflies of the Genus Ephemeropsis Eichw.(Ephemeroptera, Hexagenitidae). Entomol. Rev., 40:485-493 (transl. from Entomol. Obozhr). Chernova, O. A., 1965. Some fossil mayflies (Ephemeroptera, Misthodotidae) found in Permian deposits in the Ural Mountains. Entomol. Rev., 44:202-207 (transl. from Entomol. Obozhr). Chernova, O. A., 1969. New Early Jurassic mayflies (Ephemeroptera: Epeoromimidae and Mesonetidae). Entomol. Rev., 48:89-93 (transl. from Entomol. Obozhr).

491 Chernova, O. A., 1970. On the classification of fossil and Recent Ephemeroptera, Entomol. Rev., 49:71-81 (transl. from Entomol. Obozhr). Chernova, O. A., 1971. A mayfly (Ephemeroptera: Leptophlebiidae) from fossil resin of Cretaceous deposits in the polar regions of Siberia. Entomol. Rev., 50:346 349 (transl. from Entomol. Obozhr). Chernova, O. A., 1977. Distinctive new mayfly nymphs (Ephemeroptera: Palingeniidae and Behningiidae) from the Jurassic of Transbaikalia. Paleontol. J., 1 1 ( 2 ) : 221 226 (transl. from Paleontol. Zh.). Chernova, O. A., 1980. Otryad Ephemerida Latreille, 1 8 1 0 . In: B. B. Rohdendorf and A. P. Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175:31 36. Cummins, K. W., 1973. Trophicrelations of aquatic insects. Annu. Rev. Entomol., 18:183 206. Demoulin, G., 1971. Contribution a l'+tude morphologique, syst~matique et phylogenique des Ephemeropt~res Jurassiques. VI. L'aile post+rieure des Hexagenites Scudder, et les rapports Hexagenitidae-ChromarcyidaeOligoneuriidae. Bull. Inst. R. Sci. Nat. Belg., 47(29): 1 10. Edmunds, G. F., Jr., 1972. Biogeography and evolution of Ephemeroptera. Annu. Rev. Entomol., 17: 21-42. Fraser, F.C., 1957. A Reclassification of the Order Odonata. R. Zool. Soc. N.S.W., Sydney, 133 pp. Hennig, W., 1981. Insect Phylogeny (Translated and edited by A. C. Pont, with revisionary notes by D. Schlee and others). Wiley, New York, N.Y., 514 pp, Hubbard, M. D. and Savage, H. M., 1981. The fossil Leptophlebiidae (Ephemeroptera): a systematic and phylogenetic review. J. Paleontol., 55(4): 810-813. Hubbard, M. D. and Kukalovh-Peck, J., 1980. Permian mayfly nymphs: new taxa and systematic characters. In: J. F. Flannagan and K. E. Marshall (Editors), Advances in Ephemeroptera Biology. Plenum, New York, N.Y., pp. 19-31. Hynes, H. B. N., 1976. Biology of Plecoptera. Annu. Rev. Entomol., 21: 135-153. Illies, J., 1965. Phylogeny and zoogeography of the Plecoptera. Annu. Rev. Entomol., 10: 117-140. Kalugina, N. S., 1974. Izmeneniye podsemeistvennogo Sostava Chironomid (Diptera, Chironomidae) kak Pokazatel' vozmozhnogo Evtrophirovaniya Vodoyemov v Kontse Mesozoya. Byull. Mosk. Ova. Ispyt. Prir. Otd. Biol., 79: 45-56. Kalugina, N. S., 1976. Non-biting midges of the Subfamily Diamesiinae (Diptera, Chironomidae) from the Upper Cretaceous of the Taymyr. Paleontol. J., 10(1): 78 83 (transl. from Paleontol. Zh.). Kalugina, N. S., 1977. Paleontologicheskiye Dannye i nekotorye Voprosy Evolyutsii Culicoidea i Chironomoidea. In: Systematika i Evolyutsia dvukrylykh Naseko. mykh. Nauka, Moscow, pp. 25-30. Kalugina, N. S., 1980. Nasekomye v Vodnykh Ekosistemakh Proshlogo. In: B. B. Rohdendorf and A . P . Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175:224 240.

Kristensen, N., 1981. Phylogeny of insect orders. Annu. Rev. Entomol., 26: 135-157. Kukalovh, J., 1963. Permian insects of Moravia. 1. Miomoptera. Sb. Geol. V~d. Paleontol., 1: 7-52. Kukalov~i, J., 1964. To the morphology of the oldest known dragonfly Erasipteron larischi Pruvost 1933, V~stn. ~st~ed. l)stavu Geol., 39: 463-464. Kukalovh, J., 1968. Permian mayfly nymphs. Psyche, 75: 310-327. Kukalov~-Peck, J., 1978. Origin and evolution of insect wings, and their relationship to metamorphosis, as documented by the fossil record. J. Morphol., 156:53 125. Kukalovh-Peck, J., 1983. Origin of the insect wing and wing articulation from the arthropodan leg. Can. J. Zool., 61(7): 1618-1669. Mackay, R. J. and Wiggins, G. B., 1979. Ecological diversity in Trichoptera. Annu. Rev. Entomol., 24: 185-208. McAlpine, J. F. and Martin, J. E. H., 1969. Canadian amber - - a paleontological treasure-chest. Can. Entomol., 101(8): 819-839. Oliver, D. R., 1971. Life-history of the Chironomidae. Annu. Rev. Entomol., 16: 211-230. Olsen, R. E., Remington, C. L., Cornet, B. and Thomson, K . S . , 1978. Cyclic change in late Triassic lacustrine communities. Science, 201: 729-733. Pinto, I. D. and Purper, I., 1978. A new genus and two new species of plecopteran insects from the Triassic of Argentina. Pesquisas, 10: 77-86. Ponomarenko, A. G., 1963. Ranneyurskiye Zhuki-plavuntsy s R. Angary. Paleontol. Zh., 1963(4): 128-131. Ponomarenko, A. G., 1969. Istoricheskoye Razvitiye Zhestkokrylykh Archostemat. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 125:1 240. Ponomarenko, A. G., 1973. Mesozoic whirligig beetles (Gyrinidae, Coleoptera). Paleontol. J., 7(4): 499 506 (transl. from Paleontol. Zh.). Ponomarenko, A. G., 1975. Coptoclava (Coleoptera)- svoyeobraznyi rannemyelovoi vodnyi Zhuk iz vostochnoi Asii. In: N. N. Kramarenko (Editor), Iskopayemaya Fauni i Flora Mongolii. Nauka, Moscow, pp. 122 139. Ponomarenko, A. G., 1976. Corydalidae (Megaloptera) from the Cretaceous of Northern Asia. Entomol. Rev., 55(1): 114 122 (transl. from Entomol. Obozhr.). Ponomarenko, A. G., 1977a. Paleozoic members of the Megaloptera (Insecta). Paleontol. J., 11(1): 73-81 (transl. from Paleontol. Zh.). Ponomarenko, A. G., 1977b. Mezozoiskiye Zhestkokrylye. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 161: 1-204. Ponomarenko, A. G., 1983. Insects in Mesozoic continental reservoirs of North Asia. In: Problems of Fauna and Flora Ecology in Ancient Basins. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 194: 143-151. Ponomarenko, A. G. and Kalugina, N. S., 1980. Obschaya kharakteristika nasekomykh myestonakhozdyeniya Manlai. In: N. S. Kalugina (Editor), Rannemyelovoye Ozera Manlai. Nauka, Moscow, pp. 68-81. Popov, Y. A., 1971. Istoricheskoye Razvitiye Poluzhestkokrylykh Infraotryada Nepomorpha (Heteroptera). Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 129:1 228.

492 Popov, Y. A., 1980. Otryad Cimicida Laicharting, 1781. In: B. B. Rohdendorf and A. P. Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175: 58-68. Popov, Y. A. and Wootton, R. J., 1977. The Upper Liassic Heteroptera of Mecklenburg and Saxony. Syst. Entomol., 2(4): 333-351. Pritykina, L. N., 1968. Strekozy Karatau (Odonata). In: B. B. Rohdendorf (Editor), Yurskiye Nasekomye Karatau. Nauka, Moscow, pp. 36-54. Pritykina, L. N., 1970. Triassic and Jurassic dragonflies (Liassophlebiidae) from Soviet Central Asia. Paleontol. J., 4(1): 91-102 (transl. from Paleontol. Zh.). Pritykina, L. N., 1977. Novye Strekozy iz nizhnyemyelovykh Otlozhenii Zabaikalya i Mongolii. In: N . N . Kramarenko (Editor), Fauna, Flora i Biostratigraphia Mesozoya i Kainozoya Mongolii. Nauka, Moscow, pp. 81-96. Pritykina, L. N., 1980. Otryad Libellulida Laicharting, 1781. In: B. B. Rohdendorf and A. B. Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175: 128-134. Rasnitsyn, A. P., 1977. New Paleozoic and Mesozoic insects. Paleontol. J., 11:60-72 (transl. from Paleontol. Zh.). Rasnitsyn, A. P., 1980. Otryad Perlida Latreille, 1802. In: B. B. Rohdendorf and A. P. Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175: 154-160. Riek, E., 1971. The origin of insects. Proc 13th Int. Congr. Entomol., Moscow, 1968, 1, pp. 292-293. Riek, E., 1973. Fossil insects from the Upper Permian of Natal, South Africa. Ann. Natal Mus., 21(3): 513-532. Riek, E., 1974. Upper Triassic insects from the "Molteno" formation, South Africa. Palaeontol. Afr., 17: 19-31. Riek, E., 1976a. Fossil insects from the middle Ecca (Lower Permian) of Southern Africa. Palaeontol. Afr., 19: 145-148. Riek, E., 1976b. An unusual mayfly (Insecta: Ephemeroptera) from the Triassic of South Africa. Palaeontol. Afr., 19: 149-151. Riek, E., 1976c. New Upper Permian insects from Natal, South Africa. Ann. Natal Mus., 22(3): 755-789. Riek, E., 1976d. A new collection of insects from the Upper Triassic of South Africa. Ann. Natal Mus., 2 2 ( 3 ) : 791-820. Rohdendorf, B. B., 1964. Istoricheskoye Razvitiye dvukrylykh Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 100:1-310 (English translation, 1974, Univ. Alberta Press, 360 pp.). Rohdendorf, B. B., 1980. Otryad Muscida, Laicharting 1781. In: B. B. Rohdendorf and A. P. Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175: 112-122. Rohdendorf, B. B. and Rasnitsyn, A. P., 1980. Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175: 1-269. Ross, H. H., 1967. The evolution and past dispersal of the Trichoptera. Annu. Rev. Entomol., 12: 169-206.

Schram, F. R., 1981. Late Paleozoic crustacean communities. J. Paleontol., 55(1): 126-137. Sharov, A. G., 1953. Pervaya Nakhodka Permskoi Lichinki vislokrylogo Nasekomogo (Megaloptera) iz Kargaly. Dokl. Akad. Nauk S.S.S.R., 89(4): 731-732. Sinichenkova, I. D., 1976. New Early Cretaceous mayflies (Insecta, Ephemeroptera) from Eastern Transbaikalia. Paleontol. J., 10(2): 189-197 (transl. from Paleontol. Zh.). Sukacheva, I. D., 1973. New caddisflies (Trichoptera) from the Mesozoic of Soviet Central Asia. Paleontol. J. 7(3): 377-384 (transl. from Paleontol. Zh.). Sukacheva, I. D., 1980. Otryad Phryganeida Latreille 1810. In: B. B. Rohdendorf and A. P. Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175: 104-109. Sukacheva, I. D., 1982. Istoricheskoye Razvitiye Otryada Rucheinikov. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 197: 1-111. ~tys, P. and Sold~n, T., 1980. Retention of tracheal gills in adult Ephemeroptera and other insects. Acta Univ. Carol. Biol., 1978: 409-435. Tillyard, R. J., 1935. Upper Permian insects from New South Wales. Part V. The Order Perlaria or stoneflies. Proc. Linnaean Soc. N. S. W., 60: 385-391. Walshe, B. M., 1951. The feeding habits of certain chironomid larvae (Subfamily Tendipedinae). Proc. Zool. Soc. London, 121: 63-79. Whalley, P. E. S., 1979. New species of Protorthoptera and Protodonata (Insecta) from the Upper Carboniferous of Britain, with a comment on the origin of wings. Bull. Br. Mus. (Nat. Hist.) Geol., 32: 85-90. Whalley, P. E. S., 1985. The systematics and palaeogeography of the Lower Jurassic insects of Dorset, England. Bull. Br. Mus. (Nat. Hist.) Geol., 39(3): 107-189. Whalley, P. E. S. and Jarzembowski, E. A., 1985. Fossil insects from the lithographic limestone of Montsech (late Jurassic-early Cretaceous), Lerida Province, Spain. Bull. Br. Mus. (Nat. Hist.) Geol., 38(5): 381-412. Wilson, M. V. H., 1978. Paleogene insect faunas from Western North America, Quaest. Entomol., 14: 13-34. Wootton, R. J., 1972. The evolution of insects in fresh water ecosystems. In: R. B. Clark and R. J. Wootton (Editors), Essays in Hydrobiology. Exeter Univ. Exeter, pp. 69-82. Wootton, R. J., 1981. Paleozoic insects. Annu. Rev. Entomol., 26: 319-344. Zherikhin, B. B., 1978. Razvitiye i Smena Myelovykh i Kainozoiskikh faunisticheskikh Kompleksov Tracheinykh i Khelitseratovykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 165: 1-200. Zherikhin, B. B., 1980. Nasekomiye v Ekosystemakh sushi. In: B. B. Rohdendorf and A. P. Rasnitsyn (Editors), Istoricheskoye Razvitiye Klassa Nasekomykh. Tr. Paleontol. Inst. Akad. Nauk S.S.S.R., 175: 189-224. Zwick, P., 1973. Insecta: Plecoptera. Phylogenetisches System und Katalog. Tierreich, 94: 1-465. Zwick, P., 1979. Revision of the stonefly family Eustheniidae (Plecoptera), with emphasis on the fauna of the Australian Region. Aquatic Insects, 1: 17-50.