Phenotypic Plasticity Associated to Environmental Hypoxia in the Neotropical Serrasalmid Piaractus Mesopotamicus (Holmberg, 1887) (Characiformes: Serrasalmidae)
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Neotropical Ichthyology, 14(2): e150187, 2016 Journal homepage: www.scielo.br/ni DOI: 10.1590/1982-0224-20150187 Published online: 20 June 2016 (ISSN 1982-0224) Phenotypic plasticity associated to environmental hypoxia in the neotropical serrasalmid Piaractus mesopotamicus (Holmberg, 1887) (Characiformes: Serrasalmidae) María Alejandra Fernández-Osuna1 and Pablo Augusto Scarabotti2 Many South American characid fishes develop reversible dermal protuberances in the jaws to optimize aquatic surface respiration (ASR) during hypoxia. To date, basic aspects of this adaptation remain unknown, mainly due to the scarcity of experimental studies. In laboratory experiments, we determined time necessary for the complete formation and reversion of these structures in Piaractus mesopotamicus, and studied comparatively behavioral, morphological, and respiratory responses along gradients of dissolved oxygen (DO) concentration. Morphological changes during hypoxia consisted in dermal protuberances of lower lip, anterior border of maxillary and distal border of opercular valve, increasing the known number of structures modified. These structures developed completely in less than 6 hours and reversed in less than 3 hours. Most of observed traits showed a logistic response curve with threshold DO values between 0.90 and 2.70 mgL-1. Respiratory frequency and opercular valve development showed similar threshold values above the level of tolerance of DO, whereas ASR and dermal protuberances of the jaws showed threshold values below this level. This observation supports the functional link between these groups of behavioral and morphological traits. This study demonstrates that this species is able to modify reversibly portions of the respiratory system to optimize responses to hypoxia. Muchos peces carácidos sudamericanos desarrollan protuberancias dérmicas reversibles en las mandíbulas para optimizar la respiración acuática superficial (RAS) durante la hipoxia. Actualmente, aspectos básicos de esta adaptación permanecen desconocidos, principalmente debido a la escasez de estudios experimentales. En experiencias de laboratorio, determinamos el tiempo necesario para el desarrollo y la reversión completos de estas estructuras en Piaractus mesopotamicus, y estudiamos comparativamente respuestas conductuales, morfológicas, y respiratorias en un gradiente de concentración de oxígeno disuelto (OD). Los cambios morfológicos durante la hipoxia consistieron en protuberancias dérmicas del labio inferior, el borde anterior del maxilar, y el borde distal de la válvula opercular, incrementando el número conocido de estructuras modificadas. Éstas se desarrollaron completamente en menos de 6 horas y se revirtieron en menos de 3 horas. La mayoría de los rasgos observados siguieron una curva de respuesta logística, con valores críticos entre 0,90 y 2,70 mgL-1 de OD. La frecuencia respiratoria y el desarrollo de la válvula opercular presentaron valores críticos similares ubicados por encima del nivel de tolerancia al OD, mientras que la RAS y las protuberancias dérmicas mandibulares presentaron críticos por debajo de dicho nivel. Estas observaciones apoyan la relación funcional existente entre estos grupos de rasgos conductuales y morfológicos. Este estudio demuestra que esta especie puede modificar reversiblemente porciones del sistema respiratorio para optimizar las respuestas a la hipoxia. Keywords: Aquatic surface respiration, Characiformes, Dermal lip protuberances, Reaction norm, River floodplains. Introduction pulse in large river floodplains (Junk, 1997) is expected to favor phenotypic plasticity. Extreme temporal fluctuations in Phenotipic plasticity is the ability of an organism to dissolved oxygen (DO) are common in these environments, modify their phenotype in response to changes in the generating a wide range of adaptations and plastic responses environment (Whitman & Agrawal, 2009). It has been to cope with hypoxia (Almeida-Val et al., 2006; Chippari- proposed as a mechanism to exploit heterogeneous or Gomes et al., 2005; Rutjes, 2006; Pollock et al., 2007; changing environments (Lande, 2014). In this context, the Chapman & McKenzie, 2009). Hypoxic areas provide food environmental heterogeneity driven by the seasonal flood and refuge to adult and juvenile fish, conferring selective 1Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción (CONICET), Dr. Materi s/n, (3100) Paraná, Argentina. [email protected] 2Instituto Nacional de Limnología (CONICET-UNL), Ciudad Universitaria, (3000) Santa Fe, Argentina. [email protected] (corresponding author) 1 Neotropical Ichthyology, 14(2): e150187, 2016 2 Hypoxia-induced plasticity in Piaractus mesopotamicus advantages to species able to colonize these environments evolution (Gibert et al., 1998; Oomen & Hutchings 2015). (Domenici et al., 2007; Yamanaka et al., 2007; Anjos et Finally, the functional link between protuberance formation al., 2008; Reid et al., 2013). Given that DO exhibit wide and ASR has been mentioned in several works, but there and fine-grained variation along the time, and responses to are no studies with simultaneous quantitative analysis of hypoxia are generally costly in adaptive terms (Chapman et behavioral and morphological traits to observe relationships al., 2008), evolution should favor rapid trait reversal when and identify the functions of these traits. Then, adequately oxygen conditions are reestablished. However, this aspect designed experiments are needed to resolve these questions. has been poorly explored for hypoxia-induced traits (e.g. In this study, we used the characiform fish Piaractus Nilsson et al., 2012). mesopotamicus (Holmberg, 1887), a species typical of In aquatics environments, DO acts like a resource in frequently hypoxic floodplain environments of South the way that organisms can opt for alternative sources America, which exhibit a series of morphological and and different types of acquisition (Kramer, 1987). Most physiological adaptations to survive at low DO concentrations of species inhabiting temporally hypoxic environments (Rantin et al., 1998; Saint-Paul & Bernardinho, 1988; Severi respond to hypoxia using behavioral strategies, like aquatic et al., 1997; Kalinin et al., 2000; Leite et al., 2007). In a surface respiration (ASR) (Almeida-Val et al., 2006; Soares series of laboratory experiments we studied comparatively et al., 2006; Chapman & McKenzie, 2009; Morosawa, behavioral, morphological, and respiratory responses of 2011; Urbina et al., 2011). ASR is a widespread mechanism P. mesopotamicus along a gradient of DO concentrations. in fishes to exploit the oxygen available in the thin layer of Our objectives were 1) to determine the degree and velocity surface water, where rapid diffusion maintains high oxygen of development and reversion of several morphological concentrations even during hypoxia (Lewis, 1970; Kramer & traits, 2) to describe the shape of response of behavioral, Mehegan, 1981). Many South American characiform species morphological and respiratory responses to hypoxia and 3) optimize the performance of ASR developing reversible to compare the degree of plasticity of these traits. dermal protuberances in the jaws that improve the influx of surface water into the mouth (Winemiller, 1989; Almeida- Material and Methods Val et al., 2006; Florindo et al., 2006; Scarabotti et al., 2009, 2011). Protuberances are edematous structures (Saint-Paul & Experimental animals and laboratory conditions. Bernardinho, 1988; Saint-Paul & Soares, 1988; Scarabotti et Juveniles_ of Piaractus mesopotamicus_ (33.54- al., 2011), which develops in 2 to 4 hours and revert completely 75.50g; x=52.73g and 93-123 mm SL; x = 1 1 0 m m ) when oxygen conditions are reestablished (Branson & Hake, were kept in 100 L aquaria with aged dechlorinated tap 1972; Braum & Junk, 1982; Saint-Paul & Bernardinho, water, at 25 ºC and an artificial photoperiod of 14:10 hours of 1988). Protuberances were described formerly for the inferior light: darkness. They were fed with floating pellet food until jaw (Braum & Junk, 1982; Winemiller, 1989), although 48 hours before experiments. recent field studies suggest that a wider range of structures In each treatment, an individual 68 x 23 x 28 cm glass can exhibit plasticity during hypoxia (Scarabotti el al., 2009, aquarium was kept to a specific DO concentration. Oxygen 2011). Given that most cases of morphological plasticity are concentrations were obtained by the addition of small irreversible and long term, this adaptation constitutes a very quantities of sodium sulfide (Na2SxH20, Anedra®, with a particular case of rapid and reversible morphological change grade of 60.8% Na2S by weight) to the water (Soares & Junk, coupled to a behavioral short term response. 2000; Soares et al., 2006) 24 hours before the placement of -1 All studies which induced protuberances development fish in aquaria. We added approximately 0.16 mgL of Na2S in laboratory have used extreme hypoxia and normoxia to reduce DO in 1 mgL-1. To avoid re-oxygenation, aquaria states as treatments, without considering the effect of were hermetically sealed with plastic sheets. The period of intermediate values of DO (Braum & Junk, 1982; Saint- 24 hours was sufficient to reach stable DO concentrations for Paul & Bernardinho, 1988; Val, 1996; Sundin et al., 2000; experiments and to oxidize the sulfide added to sulfite and Florindo et al., 2006). Critical DO concentrations were sulfate products (Cline & Richards, 1969; Chen & Morris, determined