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Modifications of the Digestive Tract for Holding Air in Loricariid and Scoloplacid Catfishes

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Modifications of the Digestive Tract for Holding Air in Loricariid and Scoloplacid Catfishes Copeia, 1998(3), pp. 663-675 Modifications of the Digestive Tract for Holding Air in Loricariid and Scoloplacid Catfishes JONATHAN W. ARMBRUSTER Loricariid catfishes have evolved several modifications of the digestive tract that • appear to fWIction as accessory respiratory organs or hydrostatic organs. Adapta­ tions include an enlarged stomach in Pterygoplichthys, Liposan:us, Glyptoperichthys, Hemiancistrus annectens, Hemiancistrus maracaiboensis, HyposWmus panamensis, and Lithoxus; a U-shaped diverticulum in Rhinelepis, Pseudorinelepis, Pogonopoma, and Po­ gonopomoides; and a ringlike diverticulum in Otocinclus. Scoloplacids, closely related to loricariids, have enlarged, clear, air-filled stomachs similar to that of Lithoxus. The ability to breathe air in Otocinclus was confirmed; the ability of Lithoxus and Scoloplax to breathe air is inferred from morphology. The diverticula of Pogonopomoides and Pogonopoma are similar to swim bladders and may be used as hydrostatic organs. The various modifications of the stomach probably represent characters that define monophyletic clades. The ovaries of Lithoxus were also examined and were sho~ to have very few (15--17) mature eggs that were large (1.6-2.2 mm) for the small size of the fish (38.6-41.4 mm SL). Los bagres loricariid an desarrollado varias modificaciones del canal digestivo que aparentan fWIcionar como organos accesorios de respiracion 0 organos hidrostati­ cos. Las adaptaciones incluyen WI estomago agrandado en Pterygoplichthys, Liposar­ cus, Glyproperichthys, Hemiancistrus annectens, Hemiancistrus maracaiboensis, Hyposto­ mus panamensis, y Lithoxus; WI diverticulum en forma de U en Rhinelepis, Pseudori­ nelepis, Pogonopoma, y Pogonopomoides; y WI diverticulum en forma de circulo en Otocinclus. Scoloplacids, de relacion cercana a los loricariids, tienen estomagos cla­ ros, agrandados, llenos de aire similares a los de Lithoxus. La habilidad de respirar aire en Otocinclus fue confirmada; la habilidad de Lithoxus y Scoloplax de respirar aire es deducida por la morfologia. La diverticula de Pogonopomoides y Pogonopoma es similar a las vejigas de natacion y pueden ser usados como organos hidrostaticos. Las varias modificaciones del estomago probablemente representan caracteristicas que definan grupos monofileticos. Los ovarios de Lithoxus tambien fueron exami­ nados y fueron mostrados a tener muy pocos (15--17) huevos maduros que eran grandes (1.6-2.2 mm) por el tamafto pequeno del pescado (38.6-41.4 mm SL). HE seasonal fluctuations of tropical South above the water. To breathe air, a fish must pos­ T American rivers have profound effects sess a highly vascularized surface that can be upon the fish fauna (Goulding, 1980; Val and kept moist. Examples include the lung of lung­ Almeida-Val, 1995). In particular, those species fishes, the buccal cavity of electric eels, the skin that occupy flooded habitats risk being subject­ of anguillid eels, and the intestine of cal­ ed to hypoxic conditions in floodplain pools lichthyid catfishes (Carter and Beadle, 1931; and swamps as the rains cease and rivers dry Carter, 1957; Johansen, 1970). Most fishes that (Carter and Beadle, 1931). Fishes are able to breathe air are not obligate air breathers and survive in poorly oxygenated water using one of switch to air breathing only during times of se­ two methods to obtain oxygen. The first is to vere hypoxia. There are few obligate air breath­ utilize aquatic surface respiration. Fishes such as ers because there is usually an energetic cost in cyprinodontiforms and some characiforms (Co­ rising to the surface to gulp air and a fitness pella, Pyrrhulina, and ctenoluciids) spend most cost in that rising to the surface makes the fish of their lives at the surface; but in times of se­ more exposed and susceptible to predation vere hypoxia, even cichlids, some catfishes, and (Kramer, 1983; Kramer et al., 1983; Power, probably most other fishes will rise to the sur­ 1984). face to breathe in the surface layer (Carter and Loricariidae (suckermouthed, armored cat­ Beadle, 1931; Kramer and McClure, 1982). fishes) is one of the largest fish families in the The second method for fishes to obtain oxy­ world, with approximately 600 species distrib­ gen in hypoxic conditions is to utilize the air uted from southern Costa Rica to northern Ar- © 1998 by the American Society of Ichthyologist<; and Herpetologist<; 664 COPEIA, 1998, NO.3 gentina (Isbriicker, 1980; Nelson, 1994). backwater pools, and well-vegetated streams Throughout this range, loricariids are common (Bailey and Baskin, 1976; L. Page and M. Sabaj, in all habitats from high gradient mountain pers. comm.). Such habitats subject the fishes streams to floodplain lakes (Burgess, 1989). Oc­ to hypoxia; however, the air breathing ability of cupying such a wide range of habitats requires scoloplacids has never been demonstrated. that loricariids have an array of adaptations for Here I describe the modified stomach of Seolo­ coping with varied life-history characteristics. Of plax and suggest it is an adaptation for air particular interest are the adaptations lorica­ breathing. riids possess for life in stagnant waters of flood­ An alternative hypothesis for the develop­ plain lakes and swamps where they must ment of air sacs in loricariids is that they pro­ breathe air to survive. vide hydrostatic control oc a resonating cham­ Air breathing in some loricariids is well ber for sound production. Schaefer (1997) sug­ known. Species of Ancistrus, Chaetostoma, Dekey­ gested that the diverticulum in Otocinclus pro­ seria, Hypoptopoma, Hypostomus, Liposarcus, Rhi­ vides hydrostatic control allowing Otocinclus to nelepis, Rineloriearia, and Sturisoma have all been live among plants in the upper water column. confirmed as being capable of breathing air However, Gee (1976) found there was no buoy­ (Kramer et aI., 1983; Santos et aI., 1994; Val and ancy advantage to the air-breathing loricariids Almeida-Val, 1995). Gradwell (1971) discussed he examined (which did not include Otocinclus). the behavior of air-breathing Hypostomus and il­ The potential of the air sacs to act as resonating lustrated that, to get its mouth above the water's chambers must be kept in mind because lori­ surface to breathe air, a Hypostomus must orient cariids do make sound, but it is unknown how vertically. Gee (1976) determined that the abil­ important sound production is or whether the ity to breathe air was dependent upon the risk fish are using the air chambers for sound. Given of hypoxia faced by a species. Of the species the recurrent theme of air breathing in lorica­ Gee examined, the torrent-dwelling astroble­ rioids, it is likely that the initial adaptation of pids (the sister family to Loricariidae; Baskin, structures was for air breathing and that alter­ 1973; Schaefer, 1987; de Pinna, 1993) and Lcp­ native uses represent exaptations. toancistrus had no ability to breathe air; the rif­ During an ongoing study on the phylogeny of fle-dwelling Chaetostoma had only a slight ability the loricariid subfamily Hypostominae, the vis­ to breathe air; and the lowland, pool-dwelling cera of species in 42 loricariid genera from five Hypostomus had the best ability to breathe air. of the six subfamilies of Loricariidae (only the However, of allloricariids for which information monotypic Lithogeneinae was not examined) is available, Liposarcus is probably the best adapt­ and in Scoloplacidae were examined. Exami­ ed to breathing air. Species of Liposarcus are nation of the viscera of loricariids and scolopla­ commonly kept out of water and sold alive in cids has revealed several modifications of the fish markets and have been known to survive up digestive system. The modifications of the di­ to 30 h out of water (Val and Almeida-Val, gestive system that hold air, the presumed evo­ 1995). lution of the structures, and the phylogenetic Few studies have been published on the mor­ implications of the structures are discussed. phological adaptations loricariids possess to breathe air. Only Liposarcus and Hypostomus have MATERIALS AND METHODS been examined, and both have been found to utilize the stomach to extract oxygen (Carter The viscera removed from specimens that and Beadle, 1931; Carter, 1935; Burgess, 1989). were subsequently cleared and stained were ex­ In Hypostomus, the stomach was found to be only amined for structures that could be utilized for slightly modified in that it was larger and thin­ aerial respiration. The digestive tracts were ner than in nonair breathers (Carter, 1935). scored as either having no obvious modifica­ However, the stomach of Liposareus was found tion, a slightly enlarged stomach, or one of sev­ to be greatly expanded with the posterior por­ en extremely well-developed, air-filled pouches tion forming a long, thin sac that was much (character states are defined in the Results and more highly vascularized than in air-breathing summarized in Table 1 for loricariids). For Hypostomus (Carter and Beadle, 1931). some of the species with a well-developed respi­ Scoloplacidae, closely related to Loricariidae, ratory organ, additional specimens were dis­ consists of one genus (Seoloplax) and four di­ sected, and the intestines were removed to de­ minutive species with a maximum reported size termine the size of the respiratory organ rela­ of about 2 cm (Bailey and Baskin, 1976; Schae­ tive to the abdominal cavity and circulatory pat­ fer et aI. 1989; Schaefer, 1990). Scoloplacids are terns. Drawings were prepared using a camera fairly common among leaf litter
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