Environmental Biology of Fishes 38: 299-309,1993.

@ 1993 Kluwer Academic Publishers. Printed in the Netherlands.

Tube-snouted gymnotiform and mormyriform fishes: convergence of aspecialized foraging mode in teleosts*

"" Crispulo Marrero1 & Kirk O. Winemilleri' I Museo de Zoologia and Programa de Recursos Naturales Renovables, UNELLEZ, Guanare, estadoI Portuguesa, Venezuela 3310).:. 2 Department of Wildlife and Fisheries Sciences, 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 theirabilities to generate and perceive an electrical field that aids in orientation, prey detection, and communi-cation. Here we present evidence from comparative ecology and morphology that tube-snouted electric fishesof the genera Sternarchorhynchus (Apteronotidae) and Campylomormyrus (Mormyridae) may be uniqueamong fishes in their mode of foraging by grasp-suction. The grasp-suction mode of feeding is a specializationfor extracting immature stages of aquatic insects that burrow into, or hide within, interstitial spaces and holesin matrices of compacted clay particles that form the channel bottom of many tropical lowland rivers. Eco-morphological implications of the remarkable evolutionary convergence for this specialized mode of foragingby tube-snouted electric fishes provide a challenge to Liem's (1984, 1990) theory of separate aquatic andterrestrial 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 modes are less constrained by a less-vertebrates have led to discussions of two funda- dense and less-variable physical medium and arementally different biomechanical models of feed- associated with less behavioral 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 designs for 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 (Alexanderdependent. According to Liem, the functional mor- 1970, Barel 1983, Motta 1984). Even though suctionphology of teleost fishes stresses versatility in feed- of whole prey appears to be the predominant feed-

* Invited Editorial

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ing mode among bony fishes, teleost orobranchial Campylomormyrus (= Gnathonemus), Mormyri-morphology does not prohibit other behavioral pat - dae) exhibit an adaptive convergence in the generalterns: biting and engulfing, or ram feeding (Nyberg form and function of the trophic apparatus. These1971, Barel 1983, Winemiller & Taylor 1987). In con- evolutionary convergences seem to have been dri-trast, the predominant mode of feeding in terres- ven by selection for specialized trophic niches asso-trial vertebrates involves biting and mastication. ciated with electroreception and burrowing aquaticLiem (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 apparatuses of 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 preyon the terrestrial vertebrate model of feeding spe- capture and ingestion. We briefly reexamine Liem'scializations and resource partitioning. Assuming a (1990) hypotheses for the relationship betweenfundamental 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 tubularhypotheses that ~xplain the feeding structures ofte- snouts and feeding modes of Stemarchorhynchusleost 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) evolutionaryconvergences among fishes are rare, (3) interspecif-ic competition is relaxed among fishes and evidence Relationships of the Mormyrifonnes andfor character displacement is lacking, and (4) the Gymnotiformesfactors driving diversification in aquatic vertebratesare different than those influencing terrestrial ver- The order Mormyriformes contains two familiestebrates. Believing that little evidence had been of- and some 200 species and is most closely allied tofered to contradict these hypotheses, Liem pro- the primitive bony tongues, Osteoglossiformesposed 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 ofsee also, Werner & Hall 1976, 1977, Lauder 1983, primitive characters (pleisiomorphies) and the ab-Winemiller 1989, 1991a, 1991b, Winemiller et al. sence of 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 muscles and have an intes-ogy of feeding, fishes of the neotropical order Gym- tine that curls around the left side of the esophagusnotiformes and the African order Mormyriformes rather than the right side. Mormyriform fishes arerepresent a special case of convergent evolution entirely restricted to freshwaters of the Africanamong aquatic vertebrates (Roberts 1972, Lowe- continent (Roberts 1975). The teleost order Gym-McConnell 1975). In this paper, we present a brief notiformes comprises a phylogenetic clade with theoverview of the trophic structures and ecologies of Cypriniformes, Characiformes, and Siluriformesthese fishes and present evidence that refutes at (superorder Ostariophysi; Fink & Fink 1981). Theleast two of Liem's hypotheses concerning the dis- order Gymnotiformes contains 6 families and attinctive features of feeding ecology in fishes relative least 100 species nearly all of which are restricted toto terrestrial vertebrates. Species within the genera freshwaters of South America (Mago-Leccia 1976).of tube-snouted gymnotiform and mormyriform Five gymnotiform species occur in Panama (Gym-fishes (e.g., Stemarchorhynchus, Apteronotidae; notus carapo, Stemopygus dariensis, Hypopomus

301

a

. H

1cm

b

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 as far back as the middle Creta-tus rostratus) and two species, Gymnotus cylindri- ceous (Fink & Fink 1981). Even if no date is as-

:- GUS and Gymnotus sp., are encountered as far north signed to this evolutionary divergence of lineages,

as Guatemala (Miller 1976). we can be reasonably confident that mormyriformBased on fossil evidence and the distribution of and gymnotiform fishes evolved electrogeneration

character states among contemporary fishes, diver- independently (Roberts 1972, Kirschbaum 1984).gence between two evolutionary lineages, the pre- Minimally, we can assume that mormyriforms havesent 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 speculated on the function-fishes in South America. al morphology of prey capture by tubular-snouted

electric fishes. Roberts (1972) made the followingremarks: '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 beakforaging microhabitat jaws and feeble dentition, are structures that permit

efficient exploitation of a rich bottom fauna of smallIn addition to the capabilities for electrogenesis and worms and worm-like insect larvae (e.g., enchy-electroreception, the external bucco-cephalic mor- traids and chironomid larvae) which other fishesphology of gymnotiforms and mormyriforms re- can only use marginally or not at all'. Tables 1 and 2veals 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 offreshwaters, the Mormyriformes and Gymnoti- fishes clearly consume very similar prey spectra,

Table 1. A comparison of the principal mesohabitats utilized by adult size classes of several South American gymnotiform and Africanmormyriform 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 (1989 unpublished data for Apure River drainage populations) for gymnotiforms. Channel bottom = the bottomsubstrate 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 + +

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and following Roberts' (1972) suggestion, genera Ephemeroptera and Chironomidae (Marrero 1987,and species with convergent diets often capture 1990, Marrero et al.1987). The long tubular snout ofprey from similar microhabitats. species belonging to the gymnotiform genus Ster-

A detailed study of the microhabitat of immature narchorhynchus (Apteronotidae) is a specializedstages of aquatic insects in the channel of the Rio adaptation for probing and removing aquatic in-Apure in Venezuela revealed that Ephemeroptera sects from small holes and tunnels in these clay sub-of the family Polymitarcidae (Campsurus spp.), Tri- strates (Marrero 1987, Marrero et al. 1987).choptera of the family Hidropsichidae (Smicridea Information from foraging studies of African¥ sp., Leptonema columbianum), and Diptera of the mormyriforms (Corbet 1961, Matthes 1964, Petr

family Chironomidae either inhabit narrow tunnels 1968, Roberts & Stewart 1976, Blake 1977) indicatesof their own construction, or they occupy tiny that Ephemeroptera (e.g., Povilla sp.), Trichoptera,spaces already formed on the river bottom (Marre- and Chironomidae are their principal prey (Tablero 1990). Within the main river channel, the most 1). Although the authors of these studies did notabundant and conspicuous of the natural refugia for make specific mention of the phenomenon, it is al-aquatic insects is bottom substrate of shifting layers most certain that a large number of African aquaticof compacted clay nodules (Fig. 2). In addition to insects construct the same type of habitations asthe interstitial spaces located between individual their neotropical homologues. In all likelihood,nodules, each compacted nodule generally contains mormyriform fishes with long tubular snouts andnumerous tiny holes and spaces that serve as refugia smalljaws armed with feeble dentition (e.g., Campi-for numerous aquatic insects, especially burrowing lomormyrus tamandua) are extracting prey from

Table 2. A comparison of the principal food categories utilized by adult size classes of several South American gymnotifonn and Africanmormyrifonn genera. Table is based on infonnation sources listed in Table 1. Chiron. = chironomid larvae; Ephem. = Ephemeropteranymphs; 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::- Campylomormyrus + + +- Hippopotamyrus + + + +

Marcusenius + + +Mormyrops + +Mormyrus + + +Petrocephalus +Pollimyrus + +

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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 same way as Sternar-chorhynchus. Petr (1968) believed that C. tamanduawere able to suck burrowing aquatic insects fromcrevices through its long narrow snout (and see ad-ditional discussion of Petr's findings below).

Blake (1977) reported habitat affinities amongmormyriform fishes in Lake Kainji, a reservoir con-structed on the Niger River in Nigeria. Like Ster-narchorhynchus, Campylomormyrus tamandua ap-pears to be strongly associated with the main chan-nel of flowing rivers. Blake (1977) reported that C.tamandua was abundant in the Niger River prior toimpoundment, and that it was rare in the reservoirdue to an apparent failure to cope with lacustrineconditions. Petr (1968) reported a virtual absence ofC. tamandua in a reservoir on the Black Volta Riverin Ghana after the first year of its formation. He re-ported that C. tamandua from the river fed on amixture of rheophilic insect larvae (e.g., epheme-ropterans Leptophlebiidae, Heptageniidae, Caenisspp.) and wood burrowing Ephemeroptera and Co-leoptera (Potamodytes, Potamocares) from slowerregions of the river. Petr (1968) assumed that' C. ta-mandua can suck these (insects) out from crevicesusing its long downward-curved snout'.

Habitat selection by mormyriforms and

gymnotiforms

In the Orinoco River drainage, some gymnotiformfishes (e.g., Sternopygus macrurus) utilize a broadrange of aquatic habitats, ranging from river chan-nels to small creeks and swamps. Other Orinocogymnotiforms exhibit relatively specialized habitataffinities. For example, Sternarchorhynchus spp.normally are found only in the main channel of riv-ers (Marrero & Taphom 1991) where water currentscontinually reform the loose matrix of clay nodulesthat harbors their aquatic insect prey. In contrast,Hypopomus spp. inhabit densely vegetatedswamps, ponds, and creeks, but are never encoun-tered in large rivers with strong currents or in openwater 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 havebeen 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 gymnoti-form fishes may exhibit more specialized feedinghabits than many of the haplochromine cichlidsfrom either lakes or rivers.

Osteo-muscular structure of the head inmormyriform and gymnotiform fishes and the

Fig. 3. Schematic diagram of a generalized teleost skull showing aquatic trophic modelthe bone movements associated with jaw opening and protru-sion: a - positions of skeletal elements at jaw closure; b - posi-. .tions of elements with jaws open and protruded (based on Hilde- Bnefly stated, the feedIng apparatus of teleosts ap-brand 1988). 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 (withDiet 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 approximatelyteleosts 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 ofvery subjective, because indices of diet breadth or feeding. In terrestrial vertebrates, food is firstidentification 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 andproposed 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 relationative 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.

P Ror: AnBq. Op. op. .

Sop.On.

b O.Op.L.AP

A 2-3

S.Td

Mx

A1

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 constructedfishes possess morphologies that result in a mode of burrows and natural spaces within the clay matrixsuction feeding that could be termed 'grasp-suc- on the bottom of river channels. Stemarchorhyn-tion', or 'suction assisted by mechanical grasping'. chus is sometimes captured near the bottom ofIn 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 spaces among leafand regulates the passage of water and food into the litter and other forms of coarse organic detritus.mouth following expansion of the orobranchial The taxonomic composition of mormyriform dietschamber. In the tube-snouted electric fishes, the suggests that an analogous behavioral sequence oc-small jaws form tiny pincers used for grasping aq- curs during feeding by African Campylomormyrusuatic insects hidden inside of small openings. The as well.compact grasping jaws 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 ofand mesethmoids (Fig. 4a). In stark contrast to the suction feeding in teleosts (sensu Osse & Mullermajority of other teleosts, all bones in the anterior 1980), and to some extent presents a challenge forhead region are elongate and thin, and together the distinction between a versatile aquatic feedingform 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 substrates prior totube-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, squamate reptiles) more than

In Sternarchorhynchus, the arrangement of the the foraging mode used by most other insectivorousmuscles and tendons controlling the mobility of teleosts.these bony pincers appears to be nearly unique Lauder (1992) recently discussed the integrationamong gymnotiforms (attachment of the Al divi- of biophysics with historical biology as a means forsion of the adductor mandibulae to the maxilla is understanding the evolution of complex structures.also found in some acanthomorphs and several silu- One could hypothesize that electroreception inriforms; J.G. Lundberg personal communication). mormyriforms and gymnotiforms first evolved asAguilera (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 benthicmaxillary near the tip of the snout (Fig. 4b). In addi- areas of large lowland rivers. Alternatively, electro-tion to lengthening the snout, this manner of long- reception could have evolved as an adaptation fordistance 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 analyses may ultimatelynarchorhynchus proceeds through the following se- shed light on these alternative evolutionary scena-quence: the prey item is first grasped within 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 genusstrate via backward locomotion, and the item is Sternarchorhynchus are adaptations for extractingthen 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 discussions of ne-sion mechanism of suction. This specialized func- otropical fishes that have highlighted diet flexibilitytional morphology of the feeding apparatus allows (e.g., Knoppel1970, Saul 1975), we believe that ros-Sternarchorhynchus to extract Ephemeroptera tral morphological features associated with feeding

308

by gymnotiform fishes limits the spectrum of ex- Lake Kainji, Nigeria, with special reference to seasonal varia-ploitable prey. Potentially the tube-snouted electric tion and interspecific differences. J. Fish Bioi. 11: 315-328.f . h Id ' 1 t d .th t f Corbet, P.S.1961. The food of non-cichlid fishes in the Lake Vic-

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~~ipsf . 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 .h A. noppe, .. . rOO 0 entra mazoman IS es. mazo-

tube-snouted specIes. niana 2: 257-352.

Lauder, G. V.1983. Functional and morphological bases of troph-ic 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. Lundberg for 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 data for Tables 1 and 2 were supported by Zool. 30: 209-221. .t t th d th f th N t .

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