Acta Gcologica Lcopoldcnsia XXIV(52/53): 145-160, 2001

INFERENCES REGARDING THE FEEDING BEHA VIOR AND MORPHOECOLOGICAL PATTERNS OF FOSSIL MA YFLY NYMPHS (INSECTA, EPHEMEROPTERA) FROM THE LOWER CRETACEOUS SANTANA FORMATION OF NORTHEASTERN BRAZIL

Polegatto, C.M. 1 & Zamboni, J.C.2

1 Lab. de Entomologia Aquática, FFCLRP-USP, Av. Bandeirantes, 3900, Ribeirão Preto, SP, CEP: 104 2 Lab. de Paleontologia, FFCLRP-USP, Av. Bandeirantes, 3900, Ribeirão Preto, SP

ABSTRACT: The life habit and diet of fossil nymphs can be understanded based on the characters of their head. The mouthparts are poorly preserved, and the inferences based on the head and the habits of extant families help to obtain a "image" of the paleoecology. This work intends to show that only an simple single image of the paleoenvironment is not enough to the knowledge about fossil mouthparts and diet, thal can be enriched with the head morphology. We used here foss il s of the Santana Formation (Lower Cretaceous, northeastern Brazil) and also illustrations of species descriptions, while the conclusions regard to mouthparts were based on extant families and their phylogenetic relationship, as wcll data of functional fceding group tables. The results demonstrate that in the Santana Formation there are nymphs which feed as collectors and shreeders, such as the Hexagenitidae, and nymphs which are filterers of suspended particles, for example Oligoneuriidae and Polymitarcyidae. A discussion of the systematic of the Ephemeroidea and the possible of Santana Formation is provided. Key word: Feeding behaviour, Nymphs, Mayflies, Morphology of , Lower Cretaceous, Santana Formation, northeast Brazi l.

RESUMO: Os hábitos e a dieta de ninfas de Ephemeroptera fósseis podem ser compreendidos com base nas características de suas cabeças. As peças bucais são malpreservadas e as inferências baseadas na cabeça e nos hábitos de famíl ias atuais ajudam a obter uma "imagem" da paleoecologia. Este trabalho pretende mostrar que somente uma simples imagem do paleoambicnte não é suficiente para o conhecimento sobre peças bucais e dieta de fósseis, o que pode ser enriquecido com a morfologia da cabeça. Nós usamos aqui fósseis da Formação Santana (Cretáceo Inferi or, nordeste brasileiro) e também ilustrações de descrições de espécies. As conclusões sobre peças bucais foram baseadas em famíl ias atuais e suas relações fil ogenéticas, bem como dados de tabelas de grupos alimentares funcionais. Os resultados demonstram que, na Formação Santana, há ninfas coletoras e fragmentadoras, tais como os Hexagenitidae, e nin fas filtradoras de partículas em suspensão, por exemplo Oligoneuriidae e Polymitarcyidae. É também apresentada uma discussão da sistemática dos Ephemeroidea e dos possíveis Leptophlebiidae da Formação Santana. Palavras-chaves: Hábitos ali mentares, Ninfas, Morfologia de insetos, Cretáceo inferior, Formação Santana, Nordeste do Brasil . 146

Introduction represented by Lcptophlebiiclae, anel Oligoneuriidae, not Thc fossil nymphs of Ephemeroptera, burrowers. Although there is variations in and other ordcrs of insects, often leave poor details, the phylogenetic groups show a well records of thcir mouthparts, although dclimitcd general pattern in functional frequently the entire hcad, cycs, and other morphology. Thc collcctors anel shredders structures of the body are well preserved bear mouthparts hard and without abundant (Labandeira, 1997). However, through bristles. The fil terers-burrowers have analysis of the head proportions and their abundant bristles for filtering suspended rclationship to the body, and with the particles. The scrapers bear strong clusters of knowledge about ecology and behavior of the hard bristles and sclerotized projections. extant maytly fauna, it is possible to make Some details of these eliffe rences are found in general conclusions about the general diet of Arens ( 1989), Frochlich (1964 ), McShaffrey the fossil ephemeropteran nyrnphs, using a and McCafferty ( 1988), Polcgatto (1998), and well cleveloped theoretical basis. Strenger (1954). Consequently, one can investigate (1) the principal feeding strategies, anel (2) the dominant elict, following the established Material and Methods classification of functional feeeling groups, as outlined in Williams and Feltmate (1992). Fossil of maytly nymphs of thc Early Adelitionally, infcrcnccs can be made about Cretaceous (Aptian-Albian) Santana (3) the occupied substrate, such as leaves, Formation, collected from Araripe Basin of wood, stone, sand and silt, and (4) properties Northeastem Brazil, were examined from the of the water and of the ambient habitat. A illustrations and photographs documented in weak association can be cstablished between Martins-Neto (1996), Martins-Neto & Caldas mouthpart structure and ecological (1990), and McCaffcrty ( 1990), as well some position, but a stronger association is possible fossils were examincd. Maiscy (1990) between mouthpa11s, dict, and behavior. presented important data about the Araripe Some important works on rnouthparts, cliet Basin. Accorcling to that author, the Araripe anel ecology are Labandeira (1997), Arens Basin today forros an elevated plateau (1989, 1990, 1994). Any contributions toward (Chapada do Araripc), rcach.in g altitudes of understanding thc fccding habits of fossil between 600 and 900rn, which extends sorne Ephemeroptera shoulel involve an 200km east-west anel 70km north-south. The investigation of shape based on (1) stmctural basin contains approximately 700m of a and biomechanica1 possibilities, and (2) an Mesozoic scdimcntary sequence, thought to exploration of phylogenetic and adaptative be of Upper Jurassic and Lower Cretaceous trends. An irnportant basis is the classification age. There is a considcrablc arnount of in functional feeding groups (FFG) of aquatic lithological and paleontological data to insects, anel the knowledge about mouthparts support the view that the Crato Member of and principal habits of species which thc Santana Formation is lacustrine. represent living families. Whitin Subenvironrncnts are found, one of these is Epherneroptera, the more plesiomorphic are the deeper lake center, while the other filterer-burrowers, such as the Epherneroidea. probably represents a marginal environment. The , , , The Araripe plateau has long been a source of , and others, are collectors or spectacular fossil vcrtebrates, especially shreeders. A very specialized type consists of fishes, turtles, crocodilians, and pterosaurs. scrapers and filterers, or collcctor-filterer in Insects, plants, anel gonorhynchiform fishes rnany works, such as Cummins (1973), and is are arnong thc more common fossils 147 occuITing in Jacustrine larninated carbonates Hexagcnitid nymphs bcar in dorsal of the Crato Member. Some of these data are view spherical heads, such as Cratogenites found in BraU!} 1(1966), Brito (1984), Moraes _, corradiniae (Figure 1), Paleobaetodes et al. (1976), and Silv~(l 983). costalimai (Figure 2), and P. britai (Figure 3), The interpretation was based on the or less commonly vertically-oriented and oval photographs, draws, and fossils. The patterns heacls, inclucling Protoligoneuria limai (Fig. used in the figures 10 and 11 were establi shed 4). McCafferty (1 990) presented a photo with based on the phylogenetic of Landa and a lateral view of this species, showing the Soldán (1985), on the works about habits of baetid-like head (Figure 4, D). cach family, and on the funcLional feeding Siphlonuriclae group (FFG) of the order Epherneroptera, The Siphlonuriclae are very similar such as Edmunds etal. (1976), Illies (1968), structurally to the Baetidae, and both clades Merritt and Cummins ( 1978), Roldán-Pérez are closely related. Siphgondwanus (1988), Williams and Feltmatc ( 1992). Thus, occidentalis (Fig. 5) is hypognathous and the comparing the patterns of the extant taxa, head is relatively similar to that of regarding head shape and general habits, with Protoligoneuria limai, a rnember of the the fossi ls concluded the functional Hexagenitidae. Both species are compared morphology of the nymphs. and revicwecl by McCafferty ( 1990), who states that both specics are similar in forro and the inferences about ecological patterns The fossil nymphs of Santana for the latter are corresponding to those for S. Formation occidentalis. Oligoneuriidac The immature stages of rnayfly The Oligoneuriidae is the only fami ly spccies that were described by Martins-Neto from the Santana Formation that is (1996), Martins-Neto & Caldas (1990), and consistently associated with a lotic habitat. McCafferty (1990) from the Santana Cratoligoneuriella leonardii (Fig. 6) and Formation, are the Hexagenitidae, Colocrus indivicum (Fig. 7) are ecologically Oligoneuriidae, Siphlonuridae, , similar to extant Oligoneuriidae, and are Polyrnitarcyidae and Potamanthidae, and specialized filterers that dwell in running possibly Leptophlebiidae. Imagoes were water. recorded as wcll principally for Ephemeroidea Ephemeroidea group. The following is a brief Among thc Ephemeroidea, rcview of the occurrencc of taxa from these Caririnympha mandibulata (Epherneridae; families in the Santana Formation. Fig. 8, C), Cratonympha microcelata Hexagen i tidae (Polimitarcyidae; Fig. 8, A), and Olindinella ln thc Santana Formation, the gracilis (Pothamantidae; Fig. 8, B), inhabit Hexagenitidae is the most commonly lentic water accorcling to Martins-Neto & represented family (see Martins-Neto, 1996; Caldas (1990). For Lhe ecology of McCaffcrty, 1990). This family includes Ephemeroidea nymphs, Martins-Neto & many records in severa! regions of the Caldas ( 1990), refers to a benthic habitat with Gondwana. Interestingly, these rcgions lack silt, sand, and mucl in bottoms of streams and cxtant species that are associated to the lakes, based on Edrnuncls et al. ( 1963), Hexagenitidae, indicating that this cladc is although there is not a clcar ecological extinct. The closest extant relatives of the definition for each family. The mandibles and Hexagenitidae are the Siphlonuridae head capsule of thcse thrce specics are vcry (McCafferty, 1990). similar. 148

Leptoph lebiidae sclerotized projections. Additionally, in the A fossil of possible Leptophlebiidae prognathous heads thc mouthparts present (Fig. 9), presented by McCafferty ( 1990) is modified articulations, and the mcdian insufficiently complete for identification. portions are dorsally-oriented, as McCafferty (1990) described lhe fossil as dcmonstrated by Arens (1989), Brown (1961) possessing a "squarish head, less in Jength and Polegatto (1998). than the thorax, narrow in lhe cervical region Examinations of the functioning of and possibly hypognathous." mayíly nymphal mouthparts increasc our Other morphological data by knowledge regarding this model, and McCaffcrty (1990) assists in reconstructing demonstrate that details of the mouthparts and the paleocnvironment, such as the presence behavior of the nymphs are stereotypcd for on Hexagenitidae nymphs of cerci for each head and mouthpart shape, such as the swimming in Jentic waters such as peripheral Baetidae, of Brown ( 1961 ), and pools within streams. Moreover, it was Heptageniidae, of McShaffrey and recordcd imagoes of Oligoneuriidae, McCafferty ( 1988) and Froehlích ( 1964). The Pristiplocia rupestris, Euthyplociidae, and most specialized structures occur in possible Pothamantidae (McCafferty, 1990) mouthparts and head of the Heptageniidae, in Santana Formation. Oligoneuriidae, Leptophlebiidae, and Ephemeroidea. By contrast, the Leptohyphidae and their allies, as well as the Life Habits and Functional Morphology Baetidae-Siphlonuridae group, bcar more generalized mouthparts and heads (sec Fig. 10 Regarding paleoccology, McCafferty and 11 ). The figure 11 demonstrates some the ( 1990) states that loli e habitats of the basic types of head and mouthparts, and some immcdiate area of thc Santana Formalion are variations. evidenced by the presence of Oligoncuriidae Regarding functional feeding groups, and Euthyplociidae, and possibly thc table 1 presents our summary of such Pothamantidae. Additionally, McCafferty classification, simplified of Mcrritt and ( 1990) suggests that the possible Cummins (1978), and Williams and Fcltmate Leptophlebiidae is possibly a membcr of a (1992). group associated with a lotic habitat. Martins­ Neto (1996) described the benthos for Protoligoneuria and Cratogenites as Discussion consisting of the silty and sandy bottoms with running and shallow watcr. By contrast, the The head structures used by Martins­ scdiment substrate for the habitat occupied by Neto (1996), Martins-Neto & Caldas (1990), Paleobaetodes is stagnant shallow water and McCafferty ( 1990) in the classifícation of within vegetated lakes, "with nymphs Santana Ephemcroptera are the sarne that we swimming freely" (Martins-Neto, 1996). employ for a morphological-functional According to a previous thcoretical understanding of thc mouthparts and diet. We model, presented herein as Figure l O, thcre is suggest that biomechanically-bascd and a predictable relationship between head- and phylogcnetic charactcrs should bc used as mouthpart shape. ln this model, hypognathous basis for interpretation. To this, wc included hcads often have very basic, hard mouthparts, supplemental data about paleoenvironment by with portions well sclerotized, and without those authors. We focused principally on the abundant bristles. The prognathous heads labial and maxillary tips and the distal bear broad, specialized mouthparts, with portions of their palps, which were compared abundant bristles, and they can to prescnt also with cxtant specics in order to provide 149

Table 1 - Functional Feeding Groups of Ephemeroptera; simplificd of Mcrritt and Cummins (1978) and Williams and Feltmate (1992).

Feeding Strategy Dominant Food Structures Associated Examples Collector Gatherer Detritus, algae, Mandibles, tips of the Baetidae, fungi, leave pieces maxillac, maxillary Siphlonuriclae, and labial paJps Caeniclae, Lcptohyphidae

Filtcrcr* Suspendecl particles, Long bristlcs of thc Pol ymitarcyidae, single-celled algae maxillae, labíum or Euthyplociidae, (diatoms) mandible Heptageniidae, Oligoneuriidae Shredder Leave pieces, wood, Mandíbles, tips of the Baetidae, detritus maxillae Leptohyphidae, Polymitarcyidae Scraper single-celled algae Clusters of hard Lcptophlcbiidae, (diatoms), fine bristles, anel tooth- Heptageniidae detritus, fungi, other like projections in the biofilm associated maxillae and the matter labium

Prcdator and Mandiblcs and Leptophlebiiclae other invcrtebrates maxillae

* The filtering strategy of nymphs of the Heptageniidae, Oligoneuriidae, and Leptophlebiidae, is very diffcrcnt of those of Ephemeroidea, in structures, behavior and evolution, and is associated with scraping, such as found in Heptageniidae and Leptophlebiidae. 150 ecologically relevant characters (Fig. 1O) . Our movemcnt of robust mouthparls (see theoretical model shows that hypognathous Polegatto, 1998). hcads are associated with more generalizcd or Siphlonuridae phylogenetically basal mouthparts within the Siphgondwanus occidentalis (Fig. 5), Ephemeroptera, whereas prognathous heads based on the presence of hypognathous are related to phylogenetically derived and mouthparts, would be typically a collector, as specializcd mouthparts and contain varied well Protoligon.euria limai, a mcmber of the structures (see Fig. 10 and 11). We present Hexagenitidae, consistent wilh data provided the following ecological infcrences fo r the by McCafferty (1990). S. occidentalis has a Santana Formation Ephemeroptcra familics. hcad that, although projecting somewhat Hcxagenitidae forward anel broad in width, seems not to be Nymphs of thc Hexagcnítidae are spherical, but rather is similar to that of a hypognathous and feed as detritus collectors. grasshopper in shape. Many extant Baetidae This condition is typical of a gencralized and Siphlonuridae bcar this type of head body-form associatcd with a facultativc diet, shape. Although Lhe statemenl by McCafferty such as occurs in extant Baetidae (see Figure ( 1990) is correct because of the general 11 ). Functionally, it is not possible to similarities, which are buttrcssed by thc close characterize these mouthparts as bearing phylogenetic relationship of both fam ilies, broad regions of bristles that are inclined there are some differences in head and body allowing scraping or filtering (see McCafferty shape between these species. As a trend, it is and McShaffrey 1988, Polegatto 1998). probablc that thc Hexagenitidae would Additionall y, there are mouthpart hard present less variation in ecology and cliet than surfaces that are used for processing of solid thc Siphlonuridae, based on the spatial and food, such as in extant Leptohyphidae. For temporal distribution of Siphlonuridac anel this type of mouthparts, shredding would some but important morphological variation complement the gathering of detritus, (sce Edmunds, 1976). although the two processes are difficult to Oligoneuriidae di stinguish in many ephemeropterans, such as Morphological characters of first stage ! Cacnidae nymphs J that Cratoligoneuriella leonardii (Fig. 6) and s1multaneously employ both processes Colocrus üuiivicum (Fig. 7) correspond (Polegatto / unpublished data). Shredding closely to those of living Oligoneuriidae. apparently is associated with more spherical Colocrus indivicwn posses ses more heads, such as Cratogenites corradiniae dcveloped mouthparts and deployment of (Figure 1), Paleobaetodes costalimai (Figure rcgions with abundant bristles, attributable to 2), and P. britai (Figure 3), and occurs in the broad area mouthpart attachment observed extant Lcptohyphidae. Alternativcly, in the fossil, as wheel as a hcad largcr than Protoligoneuria limai (Fig. 4), has a more the thorax. Thus thcre is relatively detailed vertical and oval head, and illustrates the data on mouthpart structure, and not only of prcdominance of collecting as found in the head shapc. ln C. indivicwn the wide head typical Baetidae. McCafferty (1990) is more similar to those of some photographically documents a lateral view of Heptageniidae, a related group, than thc most this species, with exhibits a baetid-like head cofamilial living Oligoneuriidae. (Fig. 4, D). Moreover, the largcst, ln terestingl y, Figure 7 of McCafferty (1990) longitudinally directed heads, such as the (Fig. 7), shows a fossil in a ventral position three previously discussed species, bear a that reveals probable glossac, paraglossae, greater space for housing more extensive, and labial palps. sclcrotized mouthparts, especially mandiblcs - features which would allow more powerful 151

Ephemeroidea Figure 8, C) anel Cratonympha microcelata Within the Ephemcroidea, the (Polymitarcyidae; Figure 8, A) (Martins-Neto Polimitarcyidae and Ephcmeridae are & Caldas, 1990), appear to be burrower, associated with Jentic water by Martins-Neto corresponding to an interpretation by Bae anel & Caldas (1990), where currently burrowing McCaffcrty (1996) for extanl taxa. The mayflies are common. However, primitive ecology of Caririnympha mandibulata, species with sprawling gaits in the two discussed by Martins-Neto & Caldas (1990), families (Bae and McCafferty, 1996) and anel baseei on earlicr study by Edmunels el al. such spccies inhabit marginal Jentic habitats ( 1963), is similar to that of extant desccndant where cletrilus and val"ious items are taxa, consisting of occupation of the firm abundant, as well as lotic habitats. Regarcling bottoms of streams and lakes that are Pothamantidae, the exlant species are found composcd of silt and sandy mud (see Bae and in mixed substrales (Bae and McCafferty, McCafferty, 1996; Edmunds et al., 1976). 1996), with species occurring variously in However, thc Polymitarcyielac also occurs in sand anel muel (Edmunels, 1976), anel mixed substrate, for example pn mit1ve representing sprawling anel burrowing life­ sprawler species (Bae and McCafferty, 1996). habits, respectively. Both types of lifc-habits Olindinella gracilis, considered as a are found in the lolic habitat of McCafferty pothamantid by Martins-Neto & Caldas (1990). McCafferty (1975), also states that ( 1990) (Fig. 8, B), could bc in assigned to the North-American Ephemcroidea "sprawl another family, the Polymirtarcyidae, more than burrow", but the work of Bae anel principally because of mandibular structures, McCafferty ( 1996), on the Polymitarcyidae, [a lthough McCaffcrty ( 1990) elescribeel a Pothamantidae, Ephemeridae, and possible pothamanlid from Santana Leptophlcbiidae indicate that species with Formation]. If O. gracilis is a member of the burrower and sprawler life-habits occur in the Pothamantidae, it would have inhabited sarne genus. The Ephemeroidea are filterers mixeel substrates based on modem descendant that obtain food while the body is enclosed taxa (see Bae and McCafferty, 1996), within burrows (in burrowers) or among the thcrefore indicating that it would have been a intersticial spaces (in sprawlers). We suggest sprawler, in opposition to the inlerpretation of that therc is a diffcrence in diet, albeit weak, Martins-Neto & Caldas (1990), who belween burrowers and sprawlers. Sprawlers suggested that it colonized a silty or muddy are capable of obtaining a more varied dict, habitat. These opposing interprctation principally regarei to size, than burrowers, as highlight the problcrn the classification of O. cvidenced by the prcsence of more numerous gracilis, and indicate that most species in the bristles in Campsurus (Polymitarcyidac), than Santana Formation would be burrowers and in Campylocia (Euthyplociielac). ln not sprawlers. burrowers, lhe clypeal-gcnal region often has Leptophlebi idae projections and bristles, and the hcad is Possible Leptophlebiidae of the flalleneel; the body is soft and light in color. Santana Fonnation do not allow a robust ln sprawlers, the head is smooth and roundeel, interpretation, because the fossil specimen is and the body is robustly sclerotized and dark­ insufficiently preservcd. ln this context hued. ln fossil Ephemeroidea, the existence of another hypothesis, not suggesteel by this associalion is unique; for cxample, bodies McCafferty ( 1990), is that this fossil occurred in eliffcrent degrees of preservation bear in a non-lotic habitat attributable to thc fact varying detail of head capsule and mouthpart that the extant subfa mily Lcptophlebiinae, structure (scc Martins-Neto & Caldas, 1990). presently occurring in Central- and North Thus, in the Santana Formation, America, typically consists of sprawler Caririnympha mandibulata (Ephcmeridae; species. ~re- members of this taxon are 152

.9-~ ---... filteK and some species are predators, and oligotrophic habitats (Roldán-Pérez 1988). inhabit lentic water (see Bae and McCafferty, Thus, based on the deéttth of the running­ 1996). McCafferty ( 1990) statcs that this watcr specics in thc Santana Formation, and fossíl has a "squarish head, lesscr than the the distribution of thcse two subfamilies, this thorax, narrow in the cervical rcgion and fossil could be allocated to thc possibly hypognathous". This analysis is Atalophlebiinae. difficult to evaluate because the hcad is Other data presented by McCafferty poorly preserved. A discernable "neck" for (1990), such as the body-form of nymphal thís fossil is typical of the Atalophlebiinae, Hexagenitidae and nymphs wilh cerci which bear prognathous moulhpart, allowing designed for a swimming in calm waters such a wíder movcment of thc head (Polegatto, as pools within streams, hclp to establish the 1998). Additionally, a squarish head is Santana paleocnvironment. This rcndering is associated with prognathous heads and is in accord with our data on collector-shredding typical ín many extant Atalophlebiinae, such Hexagenitidae as well, and is consistent with as thc Hermanella group, indicating that a the presence of allochthonous organic "squarish hypognathous head" is inconsistent particulate matter in Santana inscct-bearing (see Polegalto, 1998). Howcver, thc squarish deposits and ephcmeroptcran access to hcad in the photograph of McCafferty ( 1990) peryphiton in areas with more lumínosity. could indicates that only the dorsal area of lhe Lastly, the imagoes of Oligoneuriidae, head is prescrved, and thus it would be Pristiplocia rupestris, Euthyplociidae, and inappropriate to say the head is "squarish". possible Pothamantidac (McCaffe1ty, 1990), Therefore, the head of this specimen is would suggest even an abundance of streams, similar to those of taxa such as corresponding also to the presencc of Paraleptophlebia (Leptophlebiinac), and is Atalophlebiinae and Oligoncuriidae, and the partly similar to those of some coexistence of filtering-sprawling and AtaJophlebiinae, such as Hagenulopsis. scraping-filtering spccies. Heads that are smaJler than the thorax would be more typical in lhe Leptophlebiinae and not the Atalophlebiinae (see Edmunds, 1976; Acknowledgements Bae and McCafferty, 1996; Hubbard et ai., 1992), including hypognathous species The authors are deeply grateful to Dr. similar to the Baetidac (see Edmunds et ai., Rafael Gioia Martins-Neto for lending works, 1976). An important character is the relatively photos and fossils, and the incentive for narrow body, found in Leptophlebiinae, such studying this interesting topic. The authors as Leptophlebia, and in some are grateful al so to Dr. Conrad Labandeira for Atalophlebiinac, including Hagenulopsis. If the important revicw of this work and his the Santana spccimen is a membcr of the suggestions. i Leptophlebiinae, the mouthparts would be of scraper-collector structure, based on ...... descriptions of the family (sce Figure 2). The References diet would be more generalist, as showed in Edmunds et al. ( 1976), such that mature ARENS, W., 1989. Comparative functional nymphs would have inhabited more lentic morphology of the mouthparts of strcam animais water, in contradistinction to the feeding on cpilithic algac. (Monographische Atalophlebiinac, with more specialized mouthparts for the scraping of periphyton and Beitdige). Arch. Hydrobíol. Suppl., 83(3): 253-534. for filtering suspended particles (Polegatto, _ _ _ ., 1990. Wear and tear of mouthparts: a criticai 1998). The latter case is restricted to lotic and problcm in strcam animais fccding on epilithic 153

algae. Can. J. Zoo/., 68: 1896-1 914. (Eintagsfliegcn). Handbuch der Zoo/ogie, Berlin, 4 ___., 1994. Striking eonvergencc in thc mouthpart (2)2/5: 1-63. evolution of strcam-li vi ng algac grazcrs. J. Zoo/. LABJ\NDEIRA, C.C., 1997. lnscct mouthparts: Sysr. Evol. Researeh, 32: 3 19-343. ascertaining the palcobiology of insect feeding BAE, Y.J. and MCCAFFERTY, W.P., 1996. strategies. A111111a/ Review of Eeology and Epherneroptera tusks and their cvolution. ln: Systematics, 28: 153-193. Currel/f Direetions in. Research on Ephemeroptera. LANDJ\, V. and SOLDÁN, T., 1985. Phylogcny and CORKUM, L.D. and CIBOROWSKI, J.H. (cds.). highcr classification of thc order Ephcmcroptera: a Canadian Seholars' Press Inc., Toron10, 377-405. discussion from the eomparative anatomical point BRITO, I.M., CAMPOS, O.A., and BERTINI, R.J., of view. Studie csl. Akad. Ved. 4: 1-121. 1984. Nota preliminar sobre os insetos da MARTINS-NETO, R.G., 1996. New mayflies (Insecta, Pormação Santana, Cretáceo Inferior da Chapada Ephemeroptera) from thc Santa na Formation do Araripe. ln: CONGRESSO BRJ\SILEJRO DE (Lower Cretaceous), Araripc Basin, northcastern GEOLOGIA, 32, Rio de Janeiro, 1984. Anais..... , Brazil. Revista Esparlola de Paleo11tologia, 11 (2), Rio de Janeiro, SBG: 530-535. 177-192. BROWN, D.S., 1961. The morphology anel func tioning MARTINS NETO, R.G. anel CALDAS E.B ., 1990. oí thc mouthparts of Chloeon diptem111 L. and Efê mcras escavadoras (lnsecta, Ephe rncroptera, Baetis rhoda11i (Pictet), (lnsecta, Ephemcroptera). Ephemeroidea) na Formação Santana (Cret<íceo Proceedings of the Zoological Society of london, Inferior), Bacia do Araripe, Nordeste do Brasil: 136 (2): 147-176. descrição de três novos gêneros e três novas CUMMINS, K.W., 1973. Trophic relations of aquatic espécies (ninfas). ln: SIMPÓSIO SOBRE A insects. J\11n. Rev. Entomol., 18: 183-206. BACIA DO ARARIPE E BACIAS INTERIORES EDMUNDS, G.F., ALLEN, R.K., anel PETERS, W.L., DO NORDESTE, 1, CRATO, 1990. Atas.... Rio 1963. An annotated key to the nymphs of the Claro: 265-273. fami lies anel sub-familics of mayílics MAYSEY, J. G., 1990. Stratigraphy anel depositional

(Ephemeroptera). U11iv. r~f Utah Biolog. Ser. , 13 environment of t.h e Crato Membcr (Santana ( 1): 1-55. Formation, Lower Crctaccous of N.E. Brazil). Jn: EDMUNDS, G.F., JENSEN, S.L. anel BERNER, L., GRIMALDI, D. A. (ed.). lnsects ji"om rhe Santana 1976. Tlte Mayflies of North a11d Ce11tral A111erica. Formation, l ower Cretaceous, ofBrazil. B11lleti11 of Minncapolis. University of Minnesota Prcss. 330 p. the American Museu111 of Natural History, 195: 15- FROEHLICH, C.G., 1964. Thc feceling apparatus of 19. thc nymph of Arthroplea crmge11er Bcngtsson McCAFFERTY, W.P., 1975. The burrowing mayl1ies (Ephemeroptera). Opuscula E1110111ologica, 29 (3): of the Unitcd States (Ephemeroptera: 188-208. Ephemeroidea). Trans. A111. E11t. Soe., 101 (3): 447- HUBBARD, M.D., E. DOMINGUEZ anel M.L. 503. PESCADOR, 1992. Los Ephemeroptera de la ___., 1990. Ephemeroptera. ln: GRIMALDi, D. República Argentina: un catálogo. Rev. Soe. Ent. A. (eel.). /nsects fro111 the Santana Formation, Argentina, 50 (1-4): 201-240. Lower Cretaceous, of Brazil. Bulletin of the ILLTES, J., 1968. Orelnung Ephemeroptera l\merican Museum of Natural HistOI)', 195: 20-50. 154

McSHAFFREY, D. anel McCAFFERTY, W.P., 1986. Feeding behavior of Stenacron interpu11ctatu111 (Ephemeroptera: Heptageniidac). lounwl o/ the North American llentlwlogical Society, 7 : 87-99. ___. , 1988. rceding behavior of Rhithrogena pellucida (Ephcmeroptera, Heptageniidae). Joumal of the North American Bentlzological Society, 7 (2): 87-99. M BRRITT, R.W. and CüMMTNS, K.W ., 1978. An !11troduc1io11 to the Aquatic lnsects of North America. Dubuque, Kendal/Hunt Publishers. 722 p. MORAES, J.F.S., SANTOS, J., and MASCARENHAS, J.C., 1976. Projeto Santana. Relatório final da etapa 1, Recife, DNPM/CPRM, (vol. 1), 269 p. POLEGATTO, C.M., 1998. Morfologia Funcional do Aparelho Bucal de Ninfas de Farrodes sp. (Ephemeroptera, Leptophlebiidae). São Paulo, SP. Dissertação de Mestrado. Univers idade ele São Paulo - USP, 1 12 p. ROLDÁN-PÉREZ, G., 1988. Guia para el estudio de los m.acroinvertebrados acuaticos dei Departamento de Antioquia. Bogotá. Editorial Presencia Ltda. 2 17 p. STRENGER, A., 1954. Zur Kopfmorphologie der Ephemericl enlarven. I, Ecdyonurus uncl Rhithrogena. Ôsterreichische Zoologische Zeitschrift, 4: 191-228. WILLIAMS, D.D. and FELTMJ\TE, B.W., 1992. Aquatic lnsects. Uni versity of Toronto. 358 p. 155

Figure 1 - Cratogenites corradiniae Martins-Neto, 1996, holotype. Photo by thc authors.

Figure 2 - Paleobaetodes costalimai Martins-Neto, 1996, holotypc; left, photo by the authors; right, photo by Martins-Neto ( 1996); scale bar 5mm. V\ -O\

Figure 3 - Paleobaetodes britoi Martins-Neto, 1996, holotype. Photo by Martins-Neto (1996); Figure 4 - Protoligoneuria limai, A. dorsal view, B e C. ventral view, D. lateral view, A. photo scale bar 5mm. by Martins-Neto (1996), B-D; photos by McCaffcrty (1990); scalc bar in A 5mm. '157

Figure 5 - Siphgo11dwa1111s occidentalis, photo by McCafferty ( 1990).

\

Figure 6 - Craroligoneuriella leonardii Martins-Neto, 1996, holotypc. Photo by Martins-Neto ( 1996); scale bar 5mm. 158

Figure 7 - Colocrus indivicum, photo by McCaffcrt y ( 1990).

Figure 8 - Ephemeroidea nymphs, A. Cratonympha microcelata (Ephemeridac), B. Olindinella gracilis (Pothamantide?), C. Caririnympha mandibulata (Polymitarcyidac); draws by Martins-Neto (in Martins-Neto & Caldas, 1990); scale bar Smm. 4i>?

"';:; Baetid2c e t;;;;- ..e; C...enidae ('.; tj Síphlonurida~'. & ~ e Leptolry"hidae C- :.- . ~ - c:c

A

"!:,· Vl o~ ~ · L....,,~phl.ebiidae \O /1~~ E{)het~e:.i ~ ti /. ?~·rt/' :Hcptag,cllii~ ) '.4:;;. . j) "" i . • ~t - ~ ·~ r l ~' ~ F.\J ~ i ( ) l---L

Figure 10 - Model for the relationship bctwccn hcad- and mouthparts shape. In the hypognathous typc, thc head is oval or spherical, and the mouthparts are more gcncralizcd and sclcrotized, without abundant bristles. By contrast, in the prognathous typc, thc hcad is flattened and broad, and the mouthparts are wcll spccializcd, with abundant bristles and with tooth-like projectiorn;. Thc draws does not show a specific mouthpart; they Figure 9 • Possiblc Lcptophlebiidae, only are schematical. · Atalophlebiinae nymph, photo by McCaffcrty (1990). 4 t#f-0 FC' 0 Bi. ~ 160

t:phcmcrclloidca _ '3X'. -~ \ ..... Lcptohyphidae / ~-:;, Pa n nota Trichor·yt !tidae

Cac.noidca (âl' "'-'"' Ncocphern~riclac.--.?' .- 13acl iscidac ~~- Cac nidac -----V rrosopistomatidac __ ...... r \, , -...... ~-

Bactoidca ..L~· Siplilonuridac ~ (}- ..e:: fü1ctiche ------~ Sdii~tonola Oni~ciga.st.ddac - -(J..... Atneletopsidae "'r 'd .~...... A metro pod· 1 ~t e ---~.;: l l cptaz?nioid~t . (éT Colobt,t nsc1dae ---- zy-· Oligo11curíidae- •:;;:}ft.~~ · Isonychidae \L llcptazcniidac._ç;i Z Ephcmeroidea -<...:::. Bclú11.gidác --~( Pothamantid

Leptophlcbioidea. Lcptophlcbiidae

Figure 11 - Phylogcnctic of Ephcmcroptera and some charactcrs or thc head and lhe moulhparts. ln this cladogram, by Landa and Soldán (1985), lhe schemcs reprcsent pattcrns of head and mouthparL'>, wilh simplificd cxamples of bristles clustcrs and sclcrotized projeclions. Regarding mouthparlS, lhe more spccialized mayflies are lhe Heptagenioidea, the Ephemcroidea, and lhe Leplophlebioidca, while the more basic onc are the Ephemerelloidea, the Caenoidca, and the Baeloiclea.