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Dermal Lip Protuberances Associated with Aquatic Surface Respiration in Juveniles of the Piscivorous Characid Salminus Brasiliensis (Actinopterygii: Characidae)

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Dermal Lip Protuberances Associated with Aquatic Surface Respiration in Juveniles of the Piscivorous Characid Salminus Brasiliensis (Actinopterygii: Characidae) View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by SEDICI - Repositorio de la UNLP Neotropical Ichthyology, 7(3):459-464, 2009 Copyright © 2009 Sociedade Brasileira de Ictiologia Dermal lip protuberances associated with aquatic surface respiration in juveniles of the piscivorous characid Salminus brasiliensis (Actinopterygii: Characidae) Pablo A. Scarabotti1,2, M. Julieta Parma1,3 , Javier A. López1,2 and Romina Ghirardi1,4 Some South American freshwater fishes can improve their capability of aquatic surface respiration (ASR) by developing dermal lip protuberances in the lower jaw. This adaptation was thought to be limited to omnivorous or herbivorous fishes. The present work provides the first evidence that juveniles of a piscivorous characid, Salminus brasiliensis, develop dermal lip protuberances during periods of hypoxia in floodplain ponds of the Salado River, in Argentina. The protuberance of S. brasiliensis involves dermal portions of both jaws exhibiting lateral lobes on the sides of the mouth arranged in the vertical plane. Water dissolved oxygen concentrations less than or equal to 1.05 mgl-1 were associated with a remarkable increase in lip protuberance. The lateral lobes of the protuberance in this species may limit the access of water to the anterior portion of the mouth which is positioned nearer to the oxygenated surface water during ASR. Finally, ASR, complemented with the development of dermal lip protuberances, can be considered a valuable strategy to survive in hypoxic environments, even for carnivorous fishes with elevated oxygen requirements. Alguns peixes de água doce da América do Sul podem melhorar o desempenho da respiração aquática superficial (RAS) desenvolvendo protuberâncias dérmicas labiais na mandíbula. Considerava-se que essa adaptação era limitada aos peixes onívoros ou herbívoros. Este trabalho apresenta os primeiros indícios de que juvenis de um caracídeo piscívoro, Salminus brasiliensis, desenvolvem protuberâncias dérmicas labiais durante períodos de hipoxia em lagoas de várzea do rio Salado, Argentina. As protuberâncias de S. brasiliensis envolvem porções dérmicas das duas mandíbulas e exibem lóbulos laterais ao lado da boca dispostas no plano vertical. Concentrações de oxigênio dissolvido na água, inferiores ou iguais a 1,05 mgl-1, foram associadas a um aumento notável no desenvolvimento das protuberâncias labiais. Nesta espécie os lóbulos laterais da protuberância podem limitar o acesso de água à porção anterior da boca, que está posicionada mais perto da superfície da água oxigenada durante a RAS. Finalmente, a RAS, complementada com o desenvolvimento de protuberâncias dérmicas labiais, pode ser considerada uma valiosa estratégia para a sobrevivência em ambientes hipóxicos, mesmo para peixes carnívoros com elevada demanda de oxigênio. Key words: Hypoxia, Morphological adaptation, Lip extension, Floodplain pond, Argentina. Introduction ASR performance by developing a swelling in the lower lip (Braum & Junk, 1982; Saint-Paul & Soares, 1988; Winemiller, Aquatic surface respiration (ASR) is a widespread 1989; Val & Almeida-Val, 1995). The lip swelling does not behavioral mechanism in freshwater fishes that allows the have a gas exchange function, but it has been hypothesized utilization of the relatively oxygen-rich surface water in that it prevents the mixture of the surface water with the contact with the atmosphere during environmental hypoxia hypoxic water just beneath (Val et al., 1998) and by changing (Kramer & Mehegan, 1981; Kramer & McClure, 1982; Soares the mouth opening to a more up-turned position, a better et al., 2006). Some South American freshwater fishes improve design to perform ASR (see Lewis, 1970). 1Instituto Nacional de Limnología, José Maciá 1933, 3016 Santo Tomé, Santa Fe, Argentina. [email protected] 2Universidad Autónoma de Entre Ríos, Facultad de Ciencia y Tecnología, Andrés Pazos y Corrientes, (3100) Paraná, Argentina. 3Universidad Nacional del Litoral, Facultad de Humanidades y Ciencias, Paraje el Pozo s/n, (3000) Santa Fe, Argentina. 4Instituto de Botánica ‘Carlos Spegazzini’. Avenida 53 477, (1900) La Plata Buenos Aires, Argentina. 459 460 Aquatic surface respiration in juveniles of Salminus brasiliensis To date, dermal lip protuberances associated with of environmental hypoxia. The relationship between water environmental hypoxia are known for at least twenty species dissolved oxygen and quantitative measurements of lip of South American Characiform fishes (Braum & Junk, 1982; protuberance is also described. Saint-Paul & Soares, 1988; Winemiller, 1989; Casciotta, 1995; Val & Almeida-Val, 1995). Winemiller (1989), in examining the Material and Methods dermal lip protuberances in fourteen Venezuelan species, observed that this trait was restricted to herbivorous and Sampling was carried out with seine nets (10 m length, 5 mm omnivorous fishes and argued that the structure of this mesh) every month from March 2004 to September 2005, in adaptation could impose limitations on the hunting activity semipermanent floodplain ponds in the Salado River, 2 km of piscivorous species during prey capture. upstream of the confluence with the Paraná River (31º39’46’’S The “dorado”, Salminus brasiliensis, is one of the largest 60º45’06’’W) (Fig. 1). Sampling was standardized by the number predators occurring in the Paraná River basin, reaching in of netting bouts (1 to 3) performed in each pond. In each netting some cases 1 m in standard length (Britski et al., 1999). The bout, we covered an area of approximately 200 m2. Individuals genus Salminus includes predatory salmon-like fishes (Géry, of S. brasiliensis were captured only in March and April 2004 1977). Salminus brasiliensis is a very active fish, characterized and from December 2004 to March 2005 in the floodplain areas by having high metabolic rates with elevated oxygen sampled, probably because of the migratory and reproductive consumption per unit mass (Parma de Croux, 1997). Juveniles cycles exhibited by this species at this point of La Plata basin specialize in piscivory very early in development (Rossi, 1989). (see Bechara et al., 2001). Specimens were preserved in 10% Adults generally occur in the main channel, but larvae and formalin for a period of one year and transferred to 70% ethanol, juveniles can enter the floodplain during inundation (Menni, prior to the processing of the material. The material analyzed 2004; Rossi et al., 2007), where they can experience hypoxic was deposited in the fish collection of the Instituto Nacional conditions. de Limnología (INALI) of Argentina, under the catalogue During an annual study of fish populations in an affluent numbers 1259, 1271, 1375, 1387, 1418 and 1605. Dissolved of the middle Paraná River in Argentina, several individuals oxygen and temperature were measured near the center of each of S. brasiliensis were collected from environments with pond at 20 cm depth with a YSI model 57 oxygen meter and with strong oxygen depletion (< 1 mgl-1). This work presents a mercury thermometer, respectively. To avoid bias produced evidence that juveniles of the piscivorous fish S. brasiliensis by daily variation, oxygen levels were taken between 900 and are capable of developing dermal lip swellings during periods 1100 hr, synchronously with fish sampling. Fig. 1. Map showing the location of Salado River in Santa Fe Province (Argentina) (left) and inset showing the study region (right). Shaded sectors indicate floodplain areas containing the sampled lakes. P. A. Scarabotti, M. J. Parma, J. A. López & R. Ghirardi 461 Lip measurements were performed in seventy-six Results juveniles S. brasiliensis (standard length; mean ± SD, 92 ± 42 mm, range 47-176 mm) with a digital caliper to the nearest The dermal lip extension exhibited by S. brasiliensis 0.01 mm. Lip width at the middle line of distal tip of lower jaw consisted of a lip broadening all around the lower jaw that (LW) was calculated as the distance between the outer face displayed a flattened lateral lobe directed dorsally (Fig. 3). of tooth row and the rostral border of the lip (Fig. 2). The lower lip also showed an anterior enlargement at the tip Maximum lip width (MLW) was registered at the point with of the lower jaw by which fish exhibited a slightly prognathic greatest lip development in the lower jaw over a line aspect. The upper jaw showed a similar but subtler lip perpendicular to the tooth row. Since lip protuberances can enlargement consisting of a flattened projection that affected become folded during preservation, fish were positioned only the lateral portion of the upper lip from the anterior end over a glass plate to acquire an unfolded aspect before of the maxillary bone to approximately the mid-point of its measurements. length (Fig. 3). Due to the shape of the lower lip protuberance, In order to determine the relationship between lip extension maximum lip width occurred generally at the sides of the and mouth shape, the longitudinal dimension of the mouth mouth. The microscopic examination of dermal lip was measured in eight individuals with fully developed lip protuberances showed extensive oedema in the stratum protuberances and eight individuals with normal lips. This spongiosum, with interstitial spaces significantly larger variable was quantified as the distance between the mouth compared to sections of normal lips (Fig. 4). The lateral lobe corner (the point of contact between upper and lower lip) and of the protuberance was observed as a membranous
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