Tube-Snouted Gymnotiform and Mormyriform Fishes: Convergenceof a Specialized Foraging Mode in Teleosts*

Environmental Biology of Fishes 38: 299-309,1993. @ 1993 Kluwer Academic Publishers. Printed in the Netherlands.

Tube-snouted gymnotiform and mormyriform fishes: convergenceof a specialized foraging mode in teleosts*

"" CrispuloMarrero1 & Kirk O. Winemiller i' I Museo de Zoologia and Programa de RecursosNaturales Renovables,UNELLEZ, Guanare, estado I Portuguesa,Venezuela 3310 ).:. 2 Department of Wildlife and FisheriesSciences, Texas A&M University, College Station, TX 77843-2258, t US.A.

Received 6.10.1992 Accepted 12.4.1993

Key words: Africa, Diet variability, Electrogenesis, Electroreception, Foraging, Neotropics, Paleotropics, South America

Synopsis

African mormyriform and South American gynmotiform fishes are unique among freshwater fishes in their abilities to generate and perceive an electrical field that aids in orientation, prey detection, and communication. Here we present evidencefrom comparative ecology and morphology that tube-snouted electric fishes of the genera Sternarchorhynchus (Apteronotidae) and Campylomormyrus (Mormyridae) may be unique among fishes in their mode of foraging by grasp-suction.The grasp-suctionmode of feeding is a specialization for extracting immature stagesof aquatic insectsthat burrow into, or hide within, interstitial spacesand holes in matrices of compacted clay particles that form the channel bottom of many tropical lowland rivers. Eco- morphological implications of the remarkable evolutionary convergencefor this specializedmode of foraging by tube-snouted electric fishes provide a challenge to Liem's (1984, 1990) theory of separate aquatic and terrestrial vertebrate feeding modes.

Introduction ing performance which often gives rise to general- ized diets in the field setting. In contrast, the ter- Biomechanical studies of the buccal apparatus of restrial feeding modesare lessconstrained by a less- vertebrates have led to discussionsof two funda- dense and less-variable physical medium and are mentally different biomechanical models of feed- associatedwith lessbehavioral plasticity. As a con- ..l ing, the terrestrial and the aquatic (Liem 1984, sequence, terrestrial vertebrates tend to exhibit ,I 1990). Because the functional morphology of suc- more specialized designsfor feeding (Liem 1984). 1. tion feeding in fishes depends, in part, upon drag The feeding apparatus of most teleosts approxi- .- forces and the high density and viscosity of water, mates a closed tube or cone, and'feeding is accom- these alternative models are considered medium- plished by sucking prey into the mouth (Alexander dependent. According to Liem, the functional mor- 1970,Barel 1983,Motta 1984).Even though suction phology of teleost fishes stressesversatility in feed- of whole prey appears to be the predominant feed-

* Invited Editorial 300 ing mode among bony fishes, teleost orobranchial Campylomormyrus (= Gnathonemus), Mormyri- morphologydoes not prohibit otherbehavioral pat - dae) exhibit an adaptive convergencein the general terns: biting and engulfing, or ram feeding (Nyberg form and function of the trophic apparatus. These 1971,Barel 1983,Winemiller & Taylor 1987).In con- evolutionary convergencesseem to have been dri- trast, the predominant mode of feeding in terres- ven by selection for specializedtrophic niches asso- trial vertebrates involves biting and mastication. ciated with electroreception and burrowing aquatic Liem (1990) believed that these differences be- invertebrate prey in clay sediments of river chan- tween terrestrial and aquatic feeding modes have nels. Moreover, the trophic apparatusesof Stemar- not been sufficiently appreciated, and as a conse- chorhynchus and Campylomormyrus share a pecu- quence, aquatic vertebrate ecologists have errone- liar configuration that is a departure from the tradi- ously constructed their ecological paradigm based tional suction model of the biomechanics of prey on the terrestrial vertebrate model of feeding spe- capture and ingestion. We briefly reexamine Liem's cializations and resource partitioning. Assuming a (1990) hypotheses for the relationship between fundamental divergence between aquatic and ter- feeding mode and ecological performance in tele- restrial feeding modes, Liem (1990) proposed four osts. Contrary to Liem's contention, the tubular hypothesesthat ~xplain the feeding structures ofte- snouts and feeding modes of Stemarchorhynchus leost fishes, their implications for trophic ecology, and Campylomormyrus illustrate a highly special- and their evolutionary transitions. Briefly, these hy- ized mechanism for prey capture within a distinc- potheses are: (1) opportunism in feeding and diet tive microhabitat. shifts are prevalent among fishes, (2) evolutionary convergencesamong fishes are rare, (3) interspecific competition is relaxed among fishes and evidence Relationships of the Mormyrifonnes and for character displacement is lacking, and (4) the Gymnotiformes factors driving diversification in aquatic vertebrates are different than those influencing terrestrial ver- The order Mormyriformes contains two families tebrates. Believing that little evidence had been of- and some 200 speciesand is most closely allied to fered to contradict these hypotheses, Liem pro- the primitive bony tongues, Osteoglossiformes posed that the feeding ecology of fishes is inconsis- (Nelson 1984). The clade formed by the Mormy- tent with the terrestrial ecological paradigm of com- formes/Osteoglossiformes(infradivision Osteoglo- petition, specialization, and niche partitioning (but somorpha) is characterized by the presence of see also, Werner & Hall 1976, 1977, Lauder 1983, primitive characters (pleisiomorphies) and the ab- Winemiller 1989, 1991a, 1991b, Winemiller et al. senceof many uniquely derived traits (synapomor- 1994,Yamaoka 1991). phies) that characterize more derived teleosts like In termsoftheirmodeoflocomotion,electrogen- the Percopmorpha. For example, the Osteoglosso- eration, electroreception, and functional morphol- morpha lack epipleural musclesand have an intes- ogy of feeding, fishes of the neotropical order Gym- tine that curls around the left side of the esophagus notiformes and the African order Mormyriformes rather than the right side. Mormyriform fishes are represent a special case of convergent evolution entirely restricted to freshwaters of the African among aquatic vertebrates (Roberts 1972, Lowe- continent (Roberts 1975).The teleost order Gym- McConnell 1975). In this paper, we present a brief notiformes comprisesa phylogenetic clade with the overview of the trophic structures and ecologies of Cypriniformes, Characiformes, and Siluriformes these fishes and present evidence that refutes at (superorder Ostariophysi; Fink & Fink 1981).The least two of Liem's hypothesesconcerning the dis- order Gymnotiformes contains 6 families and at tinctive features of feeding ecology in fishesrelative least 100species nearly all of which are restricted to to terrestrial vertebrates. Specieswithin the genera freshwaters of South America (Mago-Leccia 1976). of tube-snouted gymnotiform and mormyriform Five gymnotiform speciesoccur in Panama (Gym- fishes (e.g., Stemarchorhynchus, Apteronotidae; notus carapo, Stemopygus dariensis, Hypopomus 301 a

. H 1cm

.' to{cm ~. .( 'I :::.:(:~~.,.;>

Fig.]. Thbe-snouted electric fishes: a - the African mormyriform Campylomormyrus rhynchophorus (drawing based on photograph in

and teeth of S. curvirostris (b and c based on illustrations in Mago-Leccia 1976). ~

occidentalis, Eigenmannia cf. virescens,Apterono- must have occurred asfar back as the middle Creta- tus rostratus) and two species, Gymnotus cylindri- ceous (Fink & Fink 1981). Even if no date is as- :- GUSand Gymnotus sp.,are encountered as far north signed to this evolutionary divergence of lineages, as Guatemala (Miller 1976). we can be reasonably confident that mormyriform Based on fossil evidence and the distribution of and gymnotiform fishes evolved electrogeneration character statesamong contemporary fishes, diver- independently (Roberts 1972, Kirschbaum 1984). gence between two evolutionary lineages, the pre- Minimally, we can assumethat mormyriforms have sent day Osteoglossomorpha and Ostariophysi, enjoyed nearly exclusive occupation of a noctural 302 foraging/electrogeneration-reception niche in Afri- formes appear to be the only ones that contain spe- ca for at least several million years (electrogener- cies with tube-like snouts (e.g., Stemarchorhyn- ation occurs in the monotypic malapterurid catfish, chus, Campylomormyrus, Fig. 1). Malapterurus electricus), as have the gymnotiform Several authors have speculatedon the function- fishes in South America. al morphology of prey capture by tubular-snouted electric fishes. Roberts (1972) made the following remarks: 'highly peculiar and remarkably similar External bucco-cephalic morphology of trophic structures [in both orders], for example di- gymnotiforms and mormyriforms in relation to verse types of elongate tubular mouths with beak foraging microhabitat jaws and feeble dentition, are structures that permit efficient exploitation of a rich bottom fauna of small In addition to the capabilities for electrogenesisand worms and worm-like insect larvae (e.g., enchy- electroreception, the external bucco-cephalic mor- traids and chironomid larvae) which other fishes phology of gymnotiforms and mormyriforms re- can only use marginally or not at all'. Tables1 and 2 veals remarkable similarities that indicate a high summarize our compilation of information on hab- degree of convergent evolution between taxa of the itats and diets for genera within the orders Mormy- two orders. Among fish orders entirely restricted to riformes and Gymnotiformes. The two groups of freshwaters, the Mormyriformes and Gymnoti- fishes clearly consume very similar prey spectra,

Table1. A comparison of the principal mesohabitats utilized by adult size classesof several South American gymnotiform and African mormyriform genera. Table is based on information presented in Corbet (1961),Matthes (1964), Petr (1968), Bell-Cross & Minshull (1988), and Winemiller (unpublished data for Zambezi River populations) for mormyrids; and in Marrero (1987,1990),Marrero et al. (1987),and Winemiller (1989unpublished data for Apure River drainage populations) for gymnotiforms. Channel bottom =the bottom substrate of larger flowing rivers; Edge/structure =undercut banks and woody debris along river and stream margins; Backwater-open = open water areas of small creeks, lagoons, and marshes; Vegetation =densely vegetated habitats of river margins, small creeks, lagoons, and marshes. genera Habitat

Channel Bottom Edge/Structure Backwater-Open Vegetation

Gymnotiformes: Adontosternarchus + + Apteronotus + + + Eigenmannia + + + + Electrophorus + + Gymnorhamphichthys + + Gymnotus + + Hypopomus + Rhabdolichops + + + Rhamphichthys "+ + Sternarchorhamphus + + Sternarchorhynchus + Sternopygus + +

Mormyriformes: Campylomormyrus + + Hippopotamyrus + + + Marcusenius + + Mormyrops + + Mormyrus + + Petrocephalus + Pollimyrus + + 303

and following Roberts' (1972)suggestion, genera Ephemeropteraand Chironomidae (Marrero 1987, and specieswith convergentdiets often capture 1990,Marrero et al.1987).The longtubular snout of prey from similar microhabitats. speciesbelonging to the gymnotiformgenus Ster- A detailedstudy of the microhabitatof immature narchorhynchus(Apteronotidae) is a specialized stagesof aquaticinsects in the channelof the Rio adaptationfor probing and removing aquatic in- Apure in Venezuelarevealed that Ephemeroptera sectsfrom smallholes and tunnels in theseclay sub- of the family Polymitarcidae(Campsurus spp.), Tri- strates(Marrero 1987,Marrero et al. 1987). ¥ sp.,chopteraLeptonema of thecolumbianum), family Hidropsichidaeand Diptera(Smicridea of the mormyriformsInformation (Corbetfrom foraging 1961,Matthes studies of 1964, AfricanPetr family Chironomidaeeither inhabit narrow tunnels 1968,Roberts & Stewart1976, Blake 1977) indicates of their own construction,or they occupy tiny that Ephemeroptera(e.g., Povilla sp.), Trichoptera, spacesalready formed on the river bottom (Marre- and Chironomidaeare their principal prey (Table ro 1990).Within the main river channel,the most 1). Although the authorsof thesestudies did not abundantand conspicuous of the naturalrefugia for makespecific mention of the phenomenon,it is al- aquaticinsects is bottomsubstrate of shiftinglayers mostcertain that a largenumber of African aquatic of compactedclay nodules(Fig. 2). In addition to insectsconstruct the sametype of habitationsas the interstitial spaceslocated betweenindividual their neotropical homologues.In all likelihood, nodules,each compacted nodule generally contains mormyriform fisheswith long tubular snoutsand numeroustiny holesand spaces that serveas refugia smalljawsarmed with feebledentition (e.g., Campi- for numerousaquatic insects, especially burrowing lomormyrustamandua) are extractingprey from

Table2. A comparison of the principal food categories utilized by adult size classesof several South American gymnotifonn and African mormyrifonn genera. Table is based on infonnation sources listed in Table 1. Chiron. = chironomid larvae; Ephem. = Ephemeroptera nymphs; Trichop. = Trichoptera larvae; Zoopla. = microcrustacea (Cladocera, Copepoda, Ostracoda); Prawns = prawns (Decapoda); Fishes = fishes.

genera Food category

Chiron. Ephem. Trichop. Zoopla. Prawns Fishes

Gymnotifonnes: Adontosternarchus + + Apteronotus + + + Eigenmannia + + Electrophorus + Gymnorhamphichthys + Gymnotus + + Hypopomus + + Rhabdolichops + Rhamphichthys + + Sternarchorhamphus + . ,Sternarchorhynchus + Sternopygus + + +

Monnyrifonnes: -:- HippopotamyrusCampylomormyrus + + + + Marcusenius + + + Mormyrops + + Mormyrus + + + Petrocephalus + Pollimyrus + + 304

Fig. 2. Clay nodule from the bottom of the main channel of the Rio Apure near Arichuna, Apure, Venezuela on 20 February 1983. Water depth was approximately 4 m. The numerous holes and spaces in the clay particle harbor immature stages of aquatic insects. small holes and burrows in the sameway as Sternar- Blake (1977) reported habitat affinities among chorhynchus.Petr (1968)believed that C. tamandua mormyriform fishes in Lake Kainji, a reservoir con- were able to suck burrowing aquatic insects from structed on the Niger River in Nigeria. Like Ster- crevices through its long narrow snout (and see ad- narchorhynchus, Campylomormyrus tamandua ap- ditional discussionof Petr's findings below). pears to be strongly associatedwith the main channel of flowing rivers. Blake (1977)reported that C. tamandua was abundant in the Niger River prior to Habitat selection by mormyriforms and impoundment, and that it was rare in the reservoir gymnotiforms due to an apparent failure to cope with lacustrine conditions. Petr (1968)reported a virtual absenceof In the Orinoco River drainage, some gymnotiform C. tamandua in a reservoir on the Black Volta River fishes (e.g., Sternopygusmacrurus) utilize a broad in Ghana after the first year of its formation. He re- range of aquatic habitats, ranging from river chan- ported that C. tamandua from the river fed on a nels to small creeks and swamps. Other Orinoco mixture of rheophilic insect larvae (e.g., epheme- gymnotiforms exhibit relatively specialized habitat ropterans Leptophlebiidae, Heptageniidae, Caenis affinities. For example, Sternarchorhynchus spp. spp.) and wood burrowing Ephemeroptera and Co- normally are found only in the main channel of riv- leoptera (Potamodytes,Potamocares) from slower ers (Marrero & Taphom 1991)where water currents regions of the river. Petr (1968)assumed that' C. ta- continually reform the loose matrix of clay nodules mandua can suck these (insects) out from crevices that harbors their aquatic insect prey. In contrast, using its long downward-curved snout'. Hypopomus spp. inhabit densely vegetated swamps,ponds, and creeks, but are never encountered in large rivers with strong currents or in open water areas of smaller slow-flowing rivers. 305

a fishes. In this case, had the diet items been classified only as 'aquatic insects', diet variability would have been nearly zero. In contrast, Liem (1990) employ- ed a very coarse scale of classification for diet items (e.g., algae, zooplankton, insect larvae, fish) and dis- cussed the high degree of diet variability in African P.Mx. haplochromine cichlids from lacustrine habitats. On Based on a scale of food classification more similar ~~: to that of Marrero than Liem, Winemiller (1991b) Hyo. described moderate diet breadths, yet a high degree b of resource partitioning among African haplochro- mines (Serranochromis spp.) in the Zambezi River. Comparatively speaking, it appears that gymnotiform fishes may exhibit more specialized feeding habits than many of the haplochromine cichlids from either lakes or rivers.

Osteo-muscular structure of the head in mormyriform and gymnotiform fishes and the Fig.3. Schematicdiagram of a generalizedteleost skull showing aquatic trophic model the bone movementsassociated with jaw openingand protrusion:a - positionsof skeletalelements at jaw closure;b - posi-. . tionsof elementswith jaws open and protruded (based on Hilde- Bnefly stated, the feedIng apparatus of teleosts ap- brand1988). P.Mx. = premaxillary,Dn. = dentary,Mx. = maxil- proximates a closed cone that expands from muscu- lary,Op. = opercular,Hyo. = hyoid. lar action, generating negative pressure inside of the closed jaws, followed by suction of water (with Diet variability in mormyriforms and the prey item) into the buccal cavity when jaws are gymnotiforms opened (Alexander 1967,1970, Osse & Muller 1980, Motta 1984, Hildebrand 1988, Liem 1990). The The causes and consequences of diet variability moveable components of the euteleost skull that fa- have received much attention in studies of trophic cilitate inertial suction following jaw opening in- ecology. Liem (1990) proposed that the apparent clude: the bones of the hyomadibular apparatus, versatility in the feeding apparatus of teleosts (the maxillary, premaxillary, and dentary bones (Fig. 3). expanding code model) leads to the prediction that These bones are usually short with approximately teleosts should exhibit a high level of diet variabil- rectangular shapes, and are often displaced consid- ity. Comparative estimates of diet breadth can be erably from their resting positions during the act of very subjective, because indices of diet breadth or feeding. In terrestrial vertebrates, food is first identification of diet shifts are each dependent up- grasped in the jaws and manipulated in the anterior " on several factors, perhaps most importantly the part of the mouth. Food is subsequently moved pos- level of prey identification. Geene & Jaksic (1983) teriorly by the mechanical action of the tongue and proposed that classification of prey beyond the lev- hyoid apparatus, synchronized by successive ab- el of order overestimates diet variability in compar- duction and adduction of the mandible in relation ative studies involving vertebrate predators. to the cranium until the item is swallowed (Liem Marrero (1990) identified diet items from stom- 1990). ach contents to the highest degree of resolution that Species of the gymnotiform genus Sternarchor- was feasible (orders and families) and observed hynchus and the morm):riform genus Campylomor- moderate diet breadths in Rio Apure apteronotid myrus represent a variation of the traditional tele- 306

Mio. Po. Fr: a Mt Cu.

Pas.

Mes Mx. Clt. lop. PMx. Bq. Op. Pop. Ror: An.

Sop. On.

b O.Op. L.AP

A 2-3

S.Td

A 1

S.Tv

Fig. 4. Mio. = myorhabdals,Pa. = parietal, Fr. = frontal, Mt. = metapterigoid, Cu. = quadrate, Pas. = parasphenoids, Mes. = mesopterigoid, Mx. = maxillary, PMx. = premaxillary, Dn. = dentary, An. = angular, Rar. = retroarticular, lop. = interopercular, Pop. = preopercular, Op. = opercular, Sop. = subopercular, Bq. = radial branchiostegals, Clt. = cleithrum, L.Op.ant. = levator operculi anterior, D.Op. = dila- tor operculi, L.A.P. = levator arcus palatini, A, = section 1 of abductor mandibulae, A2-3 = sections 2-3 of abductor mandibulae, L.Op.post. = levator opercular posterior, S.Td. = section of dorsal tendons, S.Tv. = section of ventral tendons. 307

ost model of aquatic suction feeding. These electric nymphs and chironomid larvae from constructed fishespossess morphologies that result in a mode of burrows and natural spaceswithin the clay matrix suction feeding that could be termed 'grasp-suc- on the bottom of river channels. Stemarchorhyn- tion', or 'suction assistedby mechanical grasping'. chus is sometimes captured near the bottom of In the traditional aquatic suction model, the mouth floodplain lakes, where they probably feed on aq- forms the aperture at the tip of a cone, or cylinder, uatic insects that are hidden in spacesamong leaf and regulates the passageof water and food into the litter and other forms of coarse organic detritus. mouth following expansion of the orobranchial The taxonomic composition of mormyriform diets chamber. In the tube-snouted electric fishes, the suggeststhat an analogousbehavioral sequenceoc- small jaws form tiny pincers used for grasping aq- curs during feeding by African Campylomormyrus uatic insects hidden inside of small openings. The as well. compact graspingjaws of these fishes are formed by The grasp-suction feeding mode involves a de- a bone complex consisting of the dent aries, vomer, gree of additional complexity to the basic model of and mesethmoids (Fig. 4a). In stark contrast to the suction feeding in teleosts (sensu Osse & Muller majority of other teleosts, all bones in the anterior 1980),and to some extent presents a challenge for head region are elongate and thin, and together the distinction between a versatile aquatic feeding form a kind of narrow wedge. The jaws of these mode versus a terrestrial feeding mode that facil- tube-snouted electric fishes exhibit none of the pro- itates specialized feeding behavior (Liem 1984, trusibility that is normally encountered in suction 1990).In some respects,the grasping of prey in pin- feeding fishes. The terminal jaw bones of these cer-like jaws and extraction from substratesprior to tube-snouted electric fishes seem to be effectively its ingestion by tube-snouted electric fishes resem- fixed in such a manner that the jaws are only able to bles the foraging mode exhibited by terrestrial in- swing open and shut for grasping small prey items. sectivores(e.g., birds, squamatereptiles) more than In Sternarchorhynchus, the arrangement of the the foraging mode usedby most other insectivorous muscles and tendons controlling the mobility of teleosts. these bony pincers appears to be nearly unique Lauder (1992) recently discussedthe integration among gymnotiforms (attachment of the Al divi- of biophysics with historical biology as a meansfor sion of the adductor mandibulae to the maxilla is understanding the evolution of complex structures. also found in some acanthomorphs and severalsilu- One could hypothesize that electroreception in riforms; J.G. Lundberg personal communication). mormyriforms and gymnotiforms first evolved as Aguilera (1986) described the insertion of the ab- an adaptation for orienting, foraging, and commu- ductor mandibulae on the internal surface of the nicating in the nearly constant darkness of benthic maxillary near the tip of the snout (Fig. 4b). In addi- areasof large lowland rivers. Alternatively, electro- tion to lengthening the snout, this manner of long- reception could have evolved as an adaptation for distance connection results in the delivery of strong nocturnal foraging in shallow freshwater habitats, pressure to a small area between the pincer-like and a subset of electric fishes subsequently colo- jaws. Based on the morphological observations we nized large river bottoms to exploit abundant inver- just described, we conclude that ingestibn by Ster- tebrate prey. Phy)ogenetic analysesmay ultimately narchorhynchus proceedsthrough the following se- shed light on these alternative evolutionary scena- quence:the prey item is first graspedwithin the pin- rios. Yet clearly, the rostral morphology and grasp- cer-like jaws, the item is then pulled from the sub- suction feeding mode of the gymnotiform genus strate via backward locomotion, and the item is Sternarchorhynchusare adaptations for extracting then sucked through the tube snout into the mid- aquatic insects from the clay matrix of river bot- buccal chamber via the normal orobranchial expan- toms. Unlike a number of earlier discussionsof ne- sion mechanism of suction. This specialized func- otropical fishes that have highlighted diet flexibility tional morphology of the feeding apparatus allows (e.g., Knoppel1970, Saul 1975),we believe that ros- Sternarchorhynchus to extract Ephemeroptera tral morphological features associatedwith feeding 308 by gymnotiform fishes limits the spectrum of ex- LakeKainji, Nigeria, with special reference to seasonalvaria- ploitable prey. Potentially the tube-snouted electric tionand interspecific differences. J.Fish Bioi. 11: 315-328. ' 1 t d .th t f Corbet, P.S.1961. The food of non-cichlid fishes in the Lake Vic- f. h Id IS es cou consume prey oca e el er on op 0 ...... tona basin, with remarks on their evolution and adaptation to or burrowed wIthIn porous substrates, yet they lacustrine conditions. Proc. Zool. Soc. Lond. 136:1-101. would have nearly exclusive access to those prey Fink, S.V. & W.L. Fink. 1981.Interrelationships of the ostario- nested in burrows and holes. The limited published physan fishes (Teleostei). Zool. J. Linn. Soc. 72: 297-353. data on diets of gymnotiform and mormyriform Geene, H. w. & ~.M. Jaksic. 1983. Food-niche rel~tion~~ips f. h t th .d th t t b t d . among sympatnc predators: effect of level of prey Identlflca- IS es suppor s e I ea a u e-snou e specIes tion. Oikos 40: 151-154. eat mostly burrowing aquatic insects. Other osta- Hildebrand, M. 1988.Form and function in vertebrate feeding riophysan fishes, including short-snouted electric and locomotion. Amer. Zool. 28: 727-738. fishes, are less capable of extracting burrowing in- Kirschbaum, F. 1984.Reproduction of weakly electric teleosts: sects, and they are presumably more efficient forag- j~st another example of convergent development? Env. Bioi. b d h rf f h b h Fish.. 10: 3-14. ersa ovean ont esu ace 0 t esu stratet an K .. lHA1970 '" d fC lA . f . . noppe, .. . rOO 0 entra mazoman ISh es. A mazo- tube-snouted specIes. niana 2: 257-352. Lauder, G. V.1983.Functional and morphological basesof trophic specialization in sunfishes (Teleostei: Centrarchidae). J. Acknowledgements Morphol. 178:1-21. Lauder, G. V. 1992. Biomechanics and evolution: integrating ...... physical and historical biology in the study of complex sys- Numerous IndIVIduals assIsted In the field work, terns. pp.1-19. In: J.M. Rayner & R.J. Wootton (ed.) Biome- and special thanks go to the fishermen of the Rio chanics in Evolution, Cambridge University Press, Cam- Apure. We thank H. Lopez Rojas, D.C. Taphorn, bridge. J.E. Thomerson,and J.G. Lundbergfor reviewing Liem, K.F. 1984. Fun~tional versatility, speciation, and niche 1. d ft f th . t St ff f th h overlap: are fishes different? pp. 269-305. In: D.G. Meyers & ear Ier ra s 0 e manuscnp a 0 e p 0- J R S . kl ( d ) 11 h. I . W. h. A ...... tnc er e. rop IC nteractlons It In quatiC Eco- tographlc laboratory of the Umversldad Central de systems, AAAS Selected Symposia, Washington, D.C. Venezuela prepared Fig. 2, and line drawings were Liem, K.F. 1990.Aquatic versus terrestrial feeding modes: pos- prepared by the first author. Field studies that con- sible impacts on the trophic ecology of vertebrates. Amer. tributed t t data th for Tables d th1 and f 2 were th Nsupported t. by Zool. 30: 209-221. . 1G Lowe-McConnell, R.H.1975. Fish communItIes In tropical fresh- gran s 0 e secon au or rom e a Iona e- . . . . . waters: their distrIbutIon, ecology, and evolution. Longman ographic Society (research in Venezuela) and the Press,London. 337 pp. Fulbright International Scholars Program of the Mago-Leccia, F. 1976.Los peces gymnotiformes de Venezuela: U.S. government (research in Zambia). un estudio prelirninar para la revision del grupo en America del Sur. Ph.D. Dissertation, Universidad Central de Venezue- la, Caracas.376 pp. . Marrero, C.1987. Notas preliminares acerca de la historia nat- References cited ural de los pecesdel bajo llano. I. 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