Development of Dermal Lip Protuberances for Aquatic Surface Respiration in South American Characid Fishes

Home , Aquatic respiration, Hoplias microlepis

COfJtia.1989(2). pp. 382-390

KIRK O. WINEMILLER

Thirteen characid and one gasteropelecid fish species from a seasonal swamp- creek of the Venezuelan llanos exhibited dermal protuberances of the lower lip during periods of extreme oxygen depletion. Relative frequencies of protuberances showed large interspecific variation and were independent of fish size within species. Protuberances appeared in three basic forms, the most elaborate of which occurred in two Triportheus species. Protuberances only were present in specimens taken from waters with surface dissolved oxygen concentrations less than or equal to 1.4 ppm with corresponding bottom concentrations less than or equal to 0.8 ppm. Environmental correlates of the appearance of lip protuberances agree well with earlier findings for two Amazonian characids. All available evidence strongly suggests that dermal lip protuberances facilitate aquatic surface respiration by reducing mixing between oxygenated surface film and hypoxic water beneath during ventilation. Two other characids, Roeboides dayi and Charax gibbosus, were common during periods of extreme aquatic hypoxia, yet did not exhibit lip protuberances. Several larger, predatory characid species emigrated downstream to avoid local hypoxic conditions. Both the appearance of lip protuberances under hypoxic conditions and their reabsorption under normoxic conditions are seen as adaptive traits for surface-feeding herbivorous and omnivorous characids.

M ANY South American fishes possessres- adaptations, yet all were reported to be in good piratory adaptations that permit survival condition at the time of collection. Similarly, in periodically-hypoxic aquatic habitats (Carter only 8 of 20 species collected in the hypoxic and Beadle, 1931; Kramer et al., 1978; Kramer, waters of the Paraguayan Chaco swamps pos- 1987). Dickson and Graham (1986) recently sessedadaptations for aerial respiration (Carter demonstrated that the Panamanian erythrinid and Beadle, 1931). Hoplias microlepisis able to survive for brief time Aquatic surface respiration (ASR) has been intervals in anoxic water via anaerobic respi- suggested to be a means by which many fishes ration. Physiological acclimation to hypoxic survive during prolonged periods of aquatic hy- conditions has been demonstrated for a number poxia (Lewis, 1970; Kramer and McClure, of fish species, including HoPlias malabaricus 1982). The use of the relatively oxygen-rich (Rantin and Johansen, 1984) and Colossomamac- surface film under conditions of extreme oxy- ropomum (Saint-Paul, 1984; Saint-Paul and gen depletion may be a widespread phenome- Soares, 1987). Aerial respiration is performed non among tropical freshwater fishes lacking by many tropical fishes using highly vascular- auxiliary respiratory adaptations (Kramer and ized internal structures for gas exchange. These McClure, 1982; Kramer, 1983, 1987). In 1984, structures include the swimbladder, branchial I collected fishes at frequent intervals over a 12 chamber and gills, epithelium of the oro-pha- mo period in the Venezuelan llanos. One site ryngeal chamber, and the gut (Johansen, 1970). in particular was characterized by periodic oxy- The majority of fishes living in periodically- gen depletion in the aquatic environment. This hypoxic aquatic habitats generally do not pos- paper presents evidence that 14 South Ameri- sessadaptations for aerial respiration (Roberts, can characiform fishes develop dermal lip pro- 1972; Kramer et al., 1978; Junk et al., 1983). tuberances during periods of extreme hypoxia. For example, Beebe (1945) collected 34 fish As has been demonstrated earlier for two Am- species from a pool of liquid mud during the azonian characids (Braum and Junk, 1982; dry seasonin northeastern Venezuela. Of these, Braum, 1983a, 1983b), these fleshy protuber- only nine species possessed aerial respiratory ances can appear and disappear rapidly and ap-

@ 1989 by the American Society of Ichthyololfists and Herpetololfists WINEMILLER-CHARACID LIP PROTUBERANCES 383

~ ..s i. ._~~~:~:;;~:- CARIBBEAN SEA I Cano Mara , ~ 10° N v~v{\

Fig. 1. Map of Venezuela showing the location of Caiio Maraca within the Rio Apure drainage basin and inset showing study region.

parently function to enhance ASR by shunting ed, low-lying areas associated with low order more of the oxygenated surface film over the creeks (canos) in the llanos. During the rainy gills. The structures are formed by oedema of season, esteros are extremely productive and the hypodermal skin layer. A survey of 20 other provide important habitat for reproduction and characiform and 44 non-characiform species the early life history stagesof many llanos fishes collected at the same site over the course of a (Mago, 1970; Taphorn and Lilyestrom, 1985; year produced no evidence of mandibular pro- Winemiller, 1987a). The estero region orCano tuberances during periods of aquatic hypoxia. Maraca is gradually reduced to a series of iso- lated muddy pools during the driest months (e.g., Study site.- The investigation was made at the from January to early May). Dry season pools estero region of Callo Maraca (8°52'30"N; are blanketed by a layer of aquatic macrophytes, 69~7'40"W), a small, second-order tributary of in which Pistia stratiotes,Ludwigia helminthorrhi- the Rio Apure drainage in the state of Portu- za, Salvinia auriculata, and S. sprucei predomi- guesa, Venezuela (Fig. 1). The site is located nate. within the western llanos, or flatlands, a region characterized by savanna habitat and remnant MATERIALS AND METHODS stands of once-dominant, deciduous forest. The soils of the region are considered the best in Fishes were collected by seine (4.5 m, 3.17 Venezuela, due in part to nutrients derived from mm mesh and 17.5 m, 12.7 mm mesh), exper- Andean alluvial deposits. The region receives imental gillnet, and dipnet during every month an average of 1300 mm of rainfall per year, of 1984. An effort was made to,obtain large with about 850 mm generally falling between samples of all species present at the site during June and Sept. "Esteros" are seasonally-flood- each collecting bout (Winemiller, 1987b). I at- 384 COPEIA, 1989, NO.2

Fig. 2. Photographs of individuals exhibiting the dermal lip protuberance (left) and typical individuals (right): (A) Gephyrocharaxvalenciae (both collected Oct.; scale bar = 1.75mm), (B) Thoracocharaxstellatus (both Jan.; scale bar = 3.0 mm), (C) Astyanax bimaculatus (both Oct.; scale bar = 3.3 mm), and (D) Triportheus sp. (Dec.-left, Jan.-right; scale bar = 6.5 mm). tempted to capture fishes from all available mi- 28th of each month. I measured dissolved oxy- crohabitats within the estero (depths ranging gen with a YSI oxygen meter (recalibrated sev- from 0-1.5 m). Only data pertinent to fish res- eral times per month) beginning in March. I piration are presented here (for additional determined pH with pH paper (MCB Reagents). physico-chemical data, see Winemiller, 1987b). Most fishes examined for the present study were Fishes were preserved immediately in 15% for- taken from the permanent pool area depicted malin, transferred to 10% formalin within a pe- in Figure 1, although a few were also collected riod of 1 mo, and tranl!lf~tired to 45% isopro- from several permanent, vegetation-choked panol within a period of 1 yr. Because our pools of the scrub forest in the upper reaches current unde1'~anding of the systematics of of the estero, and a narrow channel joining the South American fishes is incomplete, distinct upper pools to the lower site. forms had to be designated as "sp." in some Each specimen was measured for SL (nearest instances (i.e., Hemigrammussp. vs H. margina- 0.1 mm) and examined for the presence of a tus). Institutional abbreviations are as listed in dermal lip protuberance. For very small speci- Le:viton et al., 1985. Voucher specimens were mens (SL ~ 30 mm), a dissecting microscope deposited in the MCNG and the TNHC. aided examination of the mandibular protu- Afternoon water temperatures and dissolved berance, which was classified as either typical oxygen concentrations were measured at the (no evidence of a protuberance), fully devel- surface and bottom at midpool on 12 principal oped (protuberance present in the most com- collection dates, occuring between the 12th and plete form characteristic of the species), or in- WINEMILLER-CHARACID LIP PROTUBERANCES 385

Aphyocharax Bryconamericus Cheirodontops Gephyrocharax Hemigrammus Odontostilbe Poptella Thoracocharax

Astyanax 8 Ctenobrycon Markiana Tetragonopterus

Fig. 4. Parasagittal histological section of the lip protuberance of Triportheus sp. (scale bar = 0.7 mm). Extensive oedema of the stratum spongiosum (SS) in the hypodermis is evident from numerous, large in- tercellular spaces (IS = interstitial spaces, EP = epi- dermis, PE = posterior edge, AS = anterior surface). c Triportheus

ance of smaller characids and Thoracocharax consisted of a soft, fleshy bulge on the distal tip of the lower jaw (Figs. 2A, B, 3A). The snouts of these fishes appear more or lessrounded when viewed dorsally. Astyanax, Ctenobrycon,Mar- kiana, and Tetragonopterusexhibited lip protu- Fig. 3. Morphology of the three characteristic lip berances that were rectangular when viewed protuberances exhibited by the Characidae and Gas- teropelecidae of the Venezuelan llanos: (A) corre- dorsally (Figs. 2C, 3B). The two Triportheus sponds to APhyocharax albumus, Bryconamericus beta, species possessedthe most elaborate lip protu- Cheirodontops geayi, GePhyrocharax valenciae, Hemigram- berances (Figs. 2D, 3C). The Triportheus lip pro- mus sp., Odontostilbe pulcher, Poptella orbicularis, Tho- tuberance is broadened laterally, and displays a racocharax stellatus; (B) corresponds to Astyanax bimac- dorso-ventrally flattened barbel on each disto- ulatus, Ctenobrycon sPilurus, Markiana geayi, lateral tip. In agreement with earlier studies Tetragonopterus argenteus; (C) corresponds to Tripor- (Braum and Junk, 1982; Braum, 1983a), his- theus sp. and Triportheus angulatus (see text for de- tological examinations of Astyanax bimaculatus, scriptions of each form). Markiana geayi, and Triportheus sp. revealed extensive oedema of the hypodermal skin layer termediate (clear evidence of a protuberance, within mandibular protuberances (Fig. 4). The but the structure was not fully developed). Stan- absence of any unusual arrangement or density dard histological methods (Humason, 1979) of blood vessels in protuberances supports were used for microscopic examination of the Braum and Junk's (1982) hypothesis that der- dermal protuberances of three species. mal enlargements perform no extraordinary gas exchange function. RESULTS Occurrence of the lip protuberances in these specieswas limited to three collection dates: 28 Thirteen species of Characidae and one Jan., 26 April, and 26 Oct. (Fig. 5). Lip pro- species from the characiform family Gastero- tuberances only were present in fishes collected pelecidae exhibited fleshy lip protuberances on from water with dissolved oxygen concentra- the distal mandibulae (Fig. 2). Morphology of tions lessthan or equal to 1.4 ppm at the surface fully-developed lip protuberances varied ac- and 0.8 ppm at the bottom (i.e., Oct.; Fig. 6). cording to species. The dermal lip protuber- Individuals possessingtypical, intermediate, and 386 COPEIA, 1989, NO.2

z 0 to 0: 0 D- O ~

.~ APH AST BAY CHE CTE GEP HEM MAR ~ POP TET TAN TAl THO APH AST BRY CHE CTE GEP HEll liAR aX> pop TET TAN TRI THO

OCTOBER .. . .. ,.0-77

o.a- 3) '8 0.6- ,~ o.s" OA- OS

0.2-

0.0"".""". APH AST BRY CHE CTE GEP HEll liAR (XX) POP TEY TAN TRI THO u~-,-,-,-, APH AST BRY CHE CTE GEP HEll liAR (XX) POP TET TAN TRI THO

SPECIES SPECIES Fig. 5. Proportion of individuals of 14 species showing typical, intermediate, and full development of dermal lip protuberances during the three periods of extreme aquatic hypoxia at Gallo Maraca contrasted with the March collection of moderate hypoxia (APH = APhyocharaxalburnus, AST = Astyanax bimaculatus, BRY = Bryconamericusbeta, GHE = Cheirodontopsgeayi, GTE = Ctenobryconspilurus, GEP = Gephyrocharax valenciae, HEM = Hemigrammus sp., MAR = Markiana geayi, ODO = Odontostilbepulcher, POP = Poptella orbicularis,. TET = Tetragonopterusl;Irgenteus, TAN = Triportheus angulatus, TRI = TriPortheus sp., THO = Thoracocharaxstellatus, total specimens examined appears above bar for each species).

fully-developed lip protuberances were present thayeri) were rare in the estero, and none were in each of three collections from extremely hyp- taken on the dates of severe aquatic hypoxia. oxic waters (Fig. 5). The proportion of specimens exhibiting protuberance development in DISCUSSION a sample (all 14 speciescombined) was inversely related to dissolved oxygen at the surface (r = Dermal lip protuberances in characids are -0.48; F = 7.3; DF = 1,26; P < 0.025) and clearly associatedwith periods of hypoxia at the near the bottom of the water column (r = - 0.40; estero of Cafio Maraca (Figs. 5, 6). Extreme F = 4.8; DF = 1,26; P < 0.05). The incidence aquatic hypoxia during Oct. and probably Jan. of lip protuberances was not significantly relat- appeared to be related to pulses of aquatic ed to fish length in 11 of 12 within-species tests macrophyte decompostition, especially of water (ANOV A) containing 10 or more individuals hyacinths (Eichhornia diversifolia). Water depths with clear evidence of lip extension develop- fell most rapidly during Jan. and Oct. relative ment. to other months. Oxygen deficiencies in the No evidence of lip protuberances was ob- main creek channel were probably influenced served in three other speciesof Characidae from primarily by microbial respiration in the drain- the Jan., April, and Oct. collections. Charax gib- ing floodplain during Jan. and Oct. The late bosusand Roeboidesdayi were common at the April sample coincided with the peak dry season site, whereas Hemigrammus marginatus was ex- in 1984. Aquatic hypoxia during April was tremely rare. The following characid species probably derived from respiration by the mac- were common in the wet season samples and rofauna within remaining small bodies of water, emigrated downstream during the dry season in addition to benthic microbial metabolism and (Jan.-May): Pygocentrusnotatus, Serrasalmus ir- possibly nocturnal respiration by submerged tis- ritans, S. rhombeus,S. medini, Mylossomaduriven- sues of floating macrophytes. iris, and Xenogoniatesbondi. Four other characids The dermal lip protuberance most likely (Acestrorhynchusmicrolepis, Colossomamacropo- serves an adaptive function during ASR, chan- mum, Piaractus brachypomus,and Gymnocorymbus neling the thin surface layer of oxygenated water WINEMILLER. .CHARACID LIP PROTUBERANCES 387

TriPortheussp. from the Venezuelan llanos also - 34. show growth and reduction of dermal lip pro- E tuberances within 24 h in aquaria (L. Nico, pers. w ~ 32- comm.). Taken together, evidence from captive 2 fishes and the correlation between incidence of 30- protuberances and natural aquatic hypoxia 28- strongly support the hypothesis that dermal lip protuberances function to enhance ASR. A sim- 26 ...... ilar function was suggested for the mandibular JAN om MARAPR MAY JUN JUL AID ~ = 101 [& 8 barbels of Osteoglossumbicirrhosum (Osteoglos- sidae) of the Amazon drainage (Kramer et al., I 1978). Unlike the lip protuberances of chara- ffi cids, the mandibular barbels of Osteoglossumare 0~ permanent structures. 0 Lewis (1970) viewed the flattened heads and w dorsally-oriented mouths of cyprinodontoid ~ fishes as adaptive during ASR, noting the prev- is alence of these forms in many North American . . . . . JAN - MAR APR MAY JUN JUL AlA; SEP OCT IDI IS; swamps where environmental hypoxia is common. Because characiform fishes frequently dominate the species-rich biotas of South Amer- ican waters, evolutionary convergences toward the cyprinodontiform head morphology to fa- ~ cilitate ASR are likely offset by selective advan- Q. tages afforded by interspecific morphological diversification in association with specialized feeding behavior (Winemiller, 1987b). Follow- ing this view, both the ability to rapidly generate JAN ~ MAR APR MAY JUN JUL A(x; ~ = 101 I:B: the lip protuberance and its reabsorption would r.«:NTH be adaptive for these fishes. Several common characid species migrated Fig. 6. Monthly temperature, dissolved oxygen, out of the estero region during periods of severe and pH levels at the estero of Callo Maraca during oxygen depletion (e.g., Pygocentrusnotatus, Ser- 1984 (all measurements were taken at the same place rasalmusspp.). Two characid speciesdid not ex- at approximately 1600 hr). hibit lip protuberances, even though they were present during one or more episodes of aquatic toward the fish's mouth while minimizing mix- hypoxia (i.e., numerous R. dayi were collected ing with the hypoxic layer beneath. Small char- on all three dates). Both species, R. dayi and acids were frequently observed swimming just Charax gibbosus,are laterally-compressed fishes below the surface throughout the dry season, with very narrow heads. The ratio of body mass although no clear distinction could be made be- to length of these fishes is low, and stealth is tween feeding and ASR. Braum and Junk (1982) their predominant form of feeding behavior. demonstrated a rapid initiation of ASR in re- Roeboides,in particular, relies upon ambush in sponse to hypoxia in laboratory-housed C. mac- order to dislodge scales from fishes using its ropomumand Bryconmelanopterum. They also ob- external snout teeth (Sazima, 1983). A lip pro- served enlargement of lower lip surface area of tuberance would likely impair this mode of Brycon only 2-3 h following the initiation of feeding. Charax is largely piscivorous in its feed- ASR. Colossomaexhibited a doubling of lip sur- ing (Winemiller, 1987b). face area following 5 h of exposure to oxygen concentrations of 0.4-0.5 ppm in the labora- Responsesof otherfishes to hypoxia.- Ten addi- tory. After a day of exposure to hypoxia, Co- tional characiform species,representing five ad- lossomalip extensions showed a second two-fold ditional families, were collected at the estero. increase in area. Upon the reestablishment of Two of the species, Leporinusfriderici and Schi- normoxic conditions, Colossomalip protuber- zodon isognathus (Anostomidae), emigrated ances showed a 70% reduction after 90 min. downstream during the onset of the dry season. 388 COPEIA, 1989, NO.2

Hoplias malabaricus, HoPlerythrinus unitaeniatus inviable mechanism for survival under pro- (Erythrinidae), Pyrrhulina lugubris, Characidium longed hypoxia for other characiform species sp 1, Characidium sp2 (Lebiasinidae), Prochilodus by virtue of their feeding ecology or head mor- mariae (Prochilodontidae), Curimata argentea, phology. Specieswith ventrally-oriented or sub- and C. cerasina(Curimatidae) all were collected terminal mouths would be restricted in their during both wet and dry seasonsand exhibited capability to utilize ASR as a respiratory strat- no evidence of lip protuberances. The smaller egy. The additional oxygen afforded by ASR species,such asPyrrhulina and Characidium spp., may facilitate feeding by surface feeders during were always captured at the pool margins among periods of severe aquatic hypoxia. Many fish vegetation and probably survive in small pock- species that lack aerial respiratory adaptations ets of more highly oxygenated water. More- reduced their feeding rates for prolonged in- over, Pyrrhulina is ecomorphologically conver- tervals during the dry season (i.e., Prochilodus gent with swamp-dwelling cyprinodontiforms mariae, Curimata argentea,H. malabaricus),as did discussed by Lewis (1970). Larger species, such speciesrelying on the gut for aerial respiration as Hoplias malabaricus and Prochilodus mariae, (i.e., Hypostomusargus, Loricarichthys typus, An- are presumed to possessphysiological adapta- cistrus sp., Corydorasspp., Hoplosternum littorale, tions for coping wth hypoxia, becausethese were see Winemiller, 1987a for data concerning the generally captured during the driest months at latter). All dry seasoncharacid specimens were midpool, below a continuous layer of floating dissected for stomach content analysis and, with aquatic vegetation. Evidence of acclimation to few exceptions, these contained food. Poten- hypoxia by H. malabaricus and the ability of a tially, body size also could influence the effec- congener, H. microlePis,to respire for brief time tiveness of ASR aided by dermal lip protuber- periods anaerobically were mentioned previ- ances. Indeed, all of the characids that exhibited ously (Rantin and Johansen, 1984; Dickson and lip protuberances at the estero were relatively Graham, 1986). HoPlerythrinus unitaeniatus pos- small species (e.g., < 10 g). Lewis (1970) hy- sessesa modified swim bladder used for aerial pothesized that aquatic respiration by large fish- respiration under hypoxic conditions (Carter es would process a volume of water at a rate in and Beadle, 1931; Graham et al., 1978; Kramer, excess of its rate of oxygen replenishment by 1978). Immediately prior to and during the 28 diffusion at the air/water interface. Yet, the Jan. collection, the estero experienced a massive first published reports of dermal lip protuber- fish die-off comprised of many large Hoplias mal- ances deal with two large herbivorous characid abaricus and a few large Astronotusocellatus and species. Machado-Allison (1982) reported der- Caquetia kraussii (Cichlidae). mal lip protuberances in juveniles of the cacha- The unusual lip protuberance was not ob- ma, Colossomamacropomum from Venezuela. He served in any of the 44 speciesbelonging to 16 suggested that the structures functioned as non-characiform families collected during the shunts during midwater plankton feeding and study. Aerial respiratory adaptations have been were lost in adult size classes.Yet, as previously reported for species belonging to five of these noted, investigators working in the central Am- families (Hypopomidae, Aspredinidae, Calli- azon region presented convincing evidence that chthyidae, Loricariidae, Synbranchidae; Kra- dermal lip protuberances in C. macropomumand mer et al., 1978). Three species from two fam- B. melanopterumdevelop in response to aquatic ilies (Poeciliidae, Cyprinodontidae) possess a hypoxia and serve to enhance ASR (Braum and morphology which was reported to preadapt Junk, 1982; Braum, 1983a, 1983b). Fish cul- members of the order (Cyprinodontiformes) for turists in the Venezuelan llanos have also re- effective utilization of the thin surface layer of ported rapid development of lip protuberances oxygen-rich water (Lewis, 1970; Kramer and in adult Colossomain association with hypoxia Mehegan, 1981). The remaining nine families in ponds ([C. aIds via] L. Nico, pers. comm.). represented at the site were as follows: Apter- Dissolved oxygen measurements are not onotidae (2 spp.), Gymnotidae (1 sp.), Rham- available for the 28 Jan. samples that exhibited phichthyidae (1 sp.), Sternopygidae (2 spp.), high frequencies of characid lip protuberances. Ageneiosidae (1 sp.), Auchenipteridae (2 spp.), The massive Hoplias die-off that occurred on Pimelodidae (7 spp.), Trichomycteridae (1 sp.), that date was observed at no other time during and Cichlidae (7 spp.). the year. Consequently, one may infer that dissolved oxygen levels were less than or equal to Potential limitations of lip protuberancefor ASR.- the lowest values recorded during other months Use of lip protuberances for ASR may be an (agro-chemical contamination or excessive hy- WINEMILLER-CHARACID LIP PROTUBERANCES 389 drogen sulfide concentrations were not sus- Development of dermal lip protuberances in pected to be primary factors in this case, and if these species represents a form of respiratory present, should have affected the smaller char- adaptation, joining anaerobic respiration and acids before the larger Hoplias and Astronotus). the list of remarkable aerial respiratory adap- Dead characids were never observed during the tations found within diverse fish taxa inhabiting course of the study. Given the limited environ- periodically oxygen-deficient habitats. mental data available, I can only conclude that dissolved oxygen values lessthan or equal to 1.4 ACKNOWLEDGMENTS ppm are necessary for the initiation of development of the lip protuberance in the fourteen This study would not have been possible with- species studied. out the field assistanceof D. Taphorn, L. Nico, Instances in which all individuals of a species A. Barbarino, P. Rodriguez, and N. Greig. D. exhibited the protuberance on a given collec- Urriola was kind enough to offer permission to tion date were rare (Fig. 5). This observation conduct the investigation on his ranch. F. Mago raises a number of questions that could be ad- L., P. Urriola M., R. Schargel, and D. Taphorn dressed by appropriately designed laboratory are gratefully acknowledged for their assistance experiments. For example, what is the critical in securing visas and permits. The Direccion level of oxygen depletion required for the de- Administacion y Desarrollo Pesquero of the velopment of the protuberance, and is it the Republic of Venezuela provided a collecting same for all species?Is there a synergistic effect permit. W. G. Reeder and the Texas Memorial of dissolved oxygen with other factors such as Museum provided assistancein the transport of temperature, pH, HIS, or nutrition levels? Do preserved specimens. I am grateful to H. Y. Van species exhibit significant geographical varia- for preparation of the histological sections. I tion in expression of the phenotype? What fac- especially thank D. Taphorn for initially iden- tors account for apparent variation in the re- tifying the fishes of Callo Maraca, logistical as- sponsiveness of individual fish within a sistance, and hospitality in Guanare. Financial population to aquatic hypoxia? The potential support was provided by National Geographic role of hormones or other biochemical factors Society grant #2765-83. in the development of lip protuberances also remains to be investigated. With this report, at least 16 South American LITERATURE CITED characiform fishes are now known to exhibit ALVAREZ DEL VILLAR, J. 1970. Pecesmexicanos. reversible lip protuberances (Braum and junk, Comision Nacional Consultiva de Pesca, Mexico 1982; Braum, 1983a, 1983b). Systematists City, Mexico. working with neotropical specimens accom- BEEBE,W. 1945. Vertebrate fauna ofa tropical dry panied by limited ecological data are cautioned season mud-hole. Zoologica 30:81-87. against using the lip protuberance or other BRAUM,E. 1983a. Beobachtungen iiber eine revers- characters with large potential for showing eco- ible lippenextension und ihre rolle bei der notat- phenotypic variation. For example, Braum mung von Bryconspec. (Pisces, Characidae) und Co- (1983b) recently placed OthonoPhaneslabiatus lossoma macropomum (Pisces, Serrasalmidae). (Steindachner 1880) in synonymy with Brycon Amazoniana 7:355-374. -. 1983b. The status of Brycon labiatus Stein- if melanopterus(Cope 1871) based on the dis- dachner 1880 (Pisces, Characoidei) and its syn- covery of the reversible lip protuberance in this onym, Othonophaneslabiatus (STEINDACHNER species. The broad, fleshy mandibular protu- 1880). Ibid. 8:265-271. berance is a principal character defining Poecilia -, AND W. J. JUNK. 1982. Morphological ad- sulphuraria (Alvarez), a speciesknown only from aptation of two Amazonian characoids (Pisces)for the Rio del Azufre (Sulphur River) in southern surviving in oxygen deficient waters. Int. Rev. Ges. Mexico (Alvarez, 1970). Hydrobiol. 67:869-886. Kramer and McClure (1982) and Kramer CARTER,G. S., AND L. C. BEADLE. 1931. The fauna (1987) concluded that ASR represents one of the swamps of the Paraguayan Chaco in relation mechanism by which many tropical fishes live to its environment II. Respiratory adaptations in the fishes. J. Linn. Soc. Lond. Zool. 37:327-368. for extended periods under hypoxic conditions. DICKSON,K. A., ANDJ. B. GRAHAM. 1986. Adapta- The earlier discovery of mandibular lip pro- tions to hypoxic environments in the erythrinid fish tuberances in two large characids and the cur- HoPlias microlePis.Env. BioI. Fish. 15:301-308. rent findings for 13 characid and one gastero- GRAHAM,J. B., D. L. KRAMERAND E. PINEDA. 1978. pelecid species support this contention. Comparative respiration of an air-breathing and 390 COPEIA, 1989, NO.2

non-air breathing characiform fish and the evolu- MACHADO-ALLISON, A. 1982. Estudios sobre la tion of aerial respiration in characins. Physiol. Zool. subfamilia Serrasalminae (Teleostei, Characidae). 51 :279-288. Parte 1. Estudio comparado de los juveniles de las HUMASON,G. L. 1979. Animal tissue techniques. W. "cashamas" de Venezuela (generos Colossomay H. Freeman Co., San Francisco, California. Piaractus). Acta BioI. Venez. 11:1-101. JOHANSEN,K. 1970. Air breathing in fishes, p. 361- MAGO L., F. 1970. Estudios preliminares sobre la 411. In: Fish physiology. Vol. 4. W. S. Hoar and D. ecologia de los peces de los llanos de Venezuela. J. Randall (eds.). Academic Press, New York, New Ibid. 7:71-102. York. RANTIN, F. T., AND K. jOHANSEN. 1984. Response JUNK, W. L., G. M. SOARESAND F. M. CARVALHO. of the teleost Hoplias malabaricus to hypoxia. Env. 1983. Distribution of fish species in a lake of the BioI. Fish. 11:221-228. Amazon river floodplain near Manaus (Lago Ca- ROBERTS,T. R. 1972. Ecology of the fishes in the ma1eao),with special reference to extreme oxygen Amazon and Congo basins. Bull. Mus Compo Zool. conditions. Amazoniana 7:397-431. Harv.143:117-147. KRAMER,D. L. 1978. Ventilation of the respiratory SAZIMA, 1. 1983. Scale-eating in characiforms and gas bladder in Hoplerythrinus unitaeniatus (Pisces, other fishes. Env. BioI. Fish. 9:87-101. Characoidei, Erythrinidae). Can. J. Zool. 56:931- SAINT-PAUL,U. 1984. Physiological adaptation to hy- 938. poxia of a neotropical characoid fish Colossomamac- -. 1983. Aquatic surface respiration in the fish- ropomum,Serrasalmidae. Ibid. 11:53-62. es of Panama: distribution in relation to risk of -, AND G. M. SOARES.1987. Diurnal distribu- hypoxia. Env. BioI. Fish. 8:49-54. tion ad behavioral responses of fishes to extreme -. 1987. Dissolved oxygen and fish behavior. hypoxia in an Amazon floodplain lake. Ibid. 20:91- Ibid. 18:81-92. 104. -, C. C. LINDSEY,G. E. E. MOODIE AND E. D. TAPHORN,D. C., AND C. G. LILYESTROM.1985. Los STEVENS.1978. The fishes and the aquatic envi- peces del Modulo "Fernando Corrales" resultados ronment of the central Amazon basin, with partic- ictiologicos del proyecto de investigacion del CON- ular reference to respiratory patterns. Can. J. Zool. lCIT-PIMA-18. Rev. Sci. Tecn. UNELLEZ 3:55- 56:717-729. 85. -, ANDJ. P. MEHEGAN. 1981. Aquatic surface WINEMILLER,K. O. 1987a. Feeding and reproductive respiration, an adaptive response to hypoxia in the biology of the currito, Hoplosternumlittorale, in the guppy, Poecilia reticulata (Pisces, Poeciliidae). Env. Venezuelan llanos with comments on the use of the BioI. Fish. 6:299-313. enlarged male pectoral spines. Env. BioI. Fish. 20: -, ANDM. MCCLURE. 1982. Aquatic surface res- 219-227. piration, a widespread adaptation to hypoxia in -. 1987b. Tests of ecomorphological and com- tropical freshwater fishes. Ibid. 7:47-55. munity level convergence among neotropical fish LEVITON, A. E., R. H. GIBBS,JR., E. HEAL AND C. E. communities. Unpubl. Ph.D. dissert., University of DAWSON.1985. Standards in herpetology and ich- Texas, Austin, Texas. thyology: part 1. Standard symbolic codes for institutional resource collections in herpetology and DEPARTMENT OF ZOOLOGY, THE UNIVERSITY OF ichthyology. Ibid. 1985(3):802-832. TEXAS, AUSTIN, TEXAS 78712. Accepted 1 LEWIS,W. M., JR. 1970. Morphological adaptations Aug. 1988. of cyprinodontoids for inhabiting oxygen deficient waters. Copeia 1970:319-326.