Morphological plasticity associated with environmental hypoxia in characiform fishes from neotropical floodplain lakes

Abstract

The ability to develop reversible dermal extensions on the lower jaw in some South American characiform fishes has been proposed as a way to optimize the performance of aquatic surface respiration (ASR) during hypoxic conditions. These structures are formed by edema of the hypodermal tissues and can develop in a large proportion of individuals inhabiting a lake within a few hours following daily changes in dissolved oxygen. Our study report the development of dermal lip protuberances in eleven species of characiform fishes associated with periods of strong environmental hypoxia in floodplain lakes of Salado River, Argentina. Protuberances occurred in different basic forms in fishes with divergent head morphology (genera Astyanax, Ctenobrycon, Aphyocharax, Brycon, Mylossoma, Triportheus, Oligosarcus and Acestrorhynchus). The discovery of dermal projections on the anterior border of maxillary bone extends the known range of structures affected by lip protuberances. Dermal structures began to develop simultaneously in both jaws below dissolved oxygen (DO) concentrations of 1.20-1.75 mgl −1 and rose in a steep manner as oxygen level decreased. The degree of morphological plasticity differed among traits and species. The shape of response of morphology to DO was similar to that previously reported on ASR, providing additional evidence about the functional link between these traits. Our results suggests that dermal lip protuberances are widely spread among characiform fishes, affecting several mouth structures. The different types of protuberances would make up for the limitations imposed by body size and mouth shape and position on the performance of ASR in fishes with divergent morphology.

Phenotypic plasticity associated to environmental hypoxia in the neotropical serrasalmid Piaractus mesopotamicus (Holmberg, 1887) (Characiformes: Serrasalmidae)

“…Additionally, it prevents the mixing of the inspired oxygenated surface water with deoxygenated water from below. Maxillary development was observed recently in other characids (Scarabotti et al, 2011) and could help preventing the ingress of less oxygenated water through the mouth corners placed more distant to the surface during ASR.…”

“…We consider that the possibilities for dermal tissue accumulation without interference in other functions are more limited in the opercular valve and in maxillary than in lower lip. However, the relative plasticity of maxillary and lower lip can differ among species with different mouth morphologies (Scarabotti et al, 2011) suggesting that selective forces can modify the degree of plasticity of different traits to optimize the performance of ASR.…”

“…ASR is a widespread mechanism in fishes to exploit the oxygen available in the thin layer of surface water, where rapid diffusion maintains high oxygen concentrations even during hypoxia (Lewis, 1970;Kramer & Mehegan, 1981). Many South American characiform species optimize the performance of ASR developing reversible dermal protuberances in the jaws that improve the influx of surface water into the mouth (Winemiller, 1989;AlmeidaVal et al, 2006;Florindo et al, 2006;Scarabotti et al, 2009Scarabotti et al, , 2011. Protuberances are edematous structures (Saint-Paul & Bernardinho, 1988;Saint-Paul & Soares, 1988;Scarabotti et al, 2011), which develops in 2 to 4 hours and revert completely when oxygen conditions are reestablished (Branson & Hake, 1972;Braum & Junk, 1982;Saint-Paul & Bernardinho, 1988).…”

“…Many South American characiform species optimize the performance of ASR developing reversible dermal protuberances in the jaws that improve the influx of surface water into the mouth (Winemiller, 1989;AlmeidaVal et al, 2006;Florindo et al, 2006;Scarabotti et al, 2009Scarabotti et al, , 2011. Protuberances are edematous structures (Saint-Paul & Bernardinho, 1988;Saint-Paul & Soares, 1988;Scarabotti et al, 2011), which develops in 2 to 4 hours and revert completely when oxygen conditions are reestablished (Branson & Hake, 1972;Braum & Junk, 1982;Saint-Paul & Bernardinho, 1988). Protuberances were described formerly for the inferior jaw (Braum & Junk, 1982;Winemiller, 1989), although recent field studies suggest that a wider range of structures can exhibit plasticity during hypoxia (Scarabotti el al., 2009(Scarabotti el al., , 2011.…”

“…Critical DO concentrations were determined in field studies with values oscillating between 1.30 and 1.75 mgL -1 , but a very high variability was observed in the response, presumably associated to environmental heterogeneity or individual differences (Winemiller, 1989;Scarabotti et al, 2011). For this reason, the response curve of dermal protuberances to DO has not been adequately established to date.…”