The Comparative Osmoregulatory Ability of Two Water Beetle Genera Whose Species Span the Fresh-Hypersaline Gradient in Inland Waters (Coleoptera: Dytiscidae, Hydrophilidae)

Abstract

A better knowledge of the physiological basis of salinity tolerance is essential to understanding the ecology and evolutionary history of organisms that have colonized inland saline waters. Coleoptera are amongst the most diverse macroinvertebrates in inland waters, including saline habitats; however, the osmoregulatory strategies they employ to deal with osmotic stress remain unexplored. Survival and haemolymph osmotic concentration at different salinities were examined in adults of eight aquatic beetle species which inhabit different parts of the fresh—hypersaline gradient. Studied species belong to two unrelated genera which have invaded saline waters independently from freshwater ancestors; Nebrioporus (Dytiscidae) and Enochrus (Hydrophilidae). Their osmoregulatory strategy (osmoconformity or osmoregulation) was identified and osmotic capacity (the osmotic gradient between the animal’s haemolymph and the external medium) was compared between species pairs co-habiting similar salinities in nature. We show that osmoregulatory capacity, rather than osmoconformity, has evolved independently in these different lineages. All species hyperegulated their haemolymph osmotic concentration in diluted waters; those living in fresh or low-salinity waters were unable to hyporegulate and survive in hyperosmotic media (> 340 mosmol kg-1). In contrast, the species which inhabit the hypo-hypersaline habitats were effective hyporegulators, maintaining their haemolymph osmolality within narrow limits (ca. 300 mosmol kg-1) across a wide range of external concentrations. The hypersaline species N. ceresyi and E. jesusarribasi tolerated conductivities up to 140 and 180 mS cm-1, respectively, and maintained osmotic gradients over 3500 mosmol kg-1, comparable to those of the most effective insect osmoregulators known to date. Syntopic species of both genera showed similar osmotic capacities and in general, osmotic responses correlated well with upper salinity levels occupied by individual species in nature. Therefore, osmoregulatory capacity may mediate habitat segregation amongst congeners across the salinity gradient.

The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles

“…However, the process of adaption to saline inland waters seems to be a unidirectional path, likely reflecting trade‐offs between competitive ability and tolerance to osmotic stress (Dunson & Travis, ; Herbst, ; Latta, Weider, Colbourne, & Pfrender, ). In general, species of Lumetus (and other beetle genera) typical of hypersaline waters are almost absent from freshwater habitats, despite been able to hyper‐regulate (Céspedes et al., ; Pallarés et al., ; Tones, )—although E. bicolor is regularly found in low mineralized waters in northern localities of Europe. Such a situation also holds for saline Hemiptera (corixids, Tones & Hammer, ), coastal and estuarine decapods (Faria et al., ; McNamara & Faria, ) and fish (Schultz & McCormick, ).…”

“…To determine the hyporegulation ability of the nine selected species (Table ), haemolymph osmolalities were measured in individuals exposed for 48 hr to different salinities within their specific tolerance ranges (as determined by pilot trials or previous work, Pallarés et al., ). All species were exposed to at least two common hyposmotic treatments (0.3 and 12 g/L) and a hyperosmotic one (35 g/L) to obtain comparable osmolality measurements.…”

“…In contrast, tolerance to the osmotic stress produced by a saline aquatic medium seems to be a very specialized secondary adaption, only present in a few insect orders (Bradley et al., ). In general, insect species that show tolerance to salinities above that of seawater are efficient hyporegulators; that is, they are able to maintain the concentration of haemolymph below that of the external medium and within a narrow range regardless of the external osmotic concentration (e.g., Herbst, Conte, & Brookes, ; Pallarés, Arribas, Bilton, Millán, & Velasco, ; Tones & Hammer, ). Ultimately, hyporegulation has the same physiological basis as mechanisms dealing with dehydration in air, as both desiccation and hyperosmotic stress alter ionic and water balance, with similar effects at the cellular level (Bradley, ; Cohen, ; Evans, ).…”

“…Here, we combine experimental, ecological and molecular data to track the evolution of desiccation resistance, hyporegulation ability and habitat transitions across the saline gradient in adults of the water beetle subgenus Lumetus . This lineage includes species in all habitat types from fresh to hypersaline waters, with differing hyporegulation abilities (Pallarés et al., ). We provide a comprehensive and generally well‐resolved phylogeny of the subgenus, together with experimental data on desiccation resistance and hyporegulation ability across its constituent taxa, and use ancestral trait reconstruction and phylogenetic comparative methods to test the following alternative hypotheses: The hyporegulation ability allowing the colonization of saline waters was co‐opted from physiological mechanisms evolved originally for desiccation resistance. The development of hyporegulation ability in saline waters was the primary adaptation, secondarily leading to an increase in desiccation resistance. Desiccation resistance and hyporegulation ability evolved in correlation. …”

The ecology of narrow-range endemic macro-invertebrates of Great Artesian Basin springs

“…Adaptations concerning tolerance of desiccation and high salinity go hand-in-hand for inland species. For example in aquatic beetles, salinity tolerance and desiccation tolerance vary across taxa (Pallarés et al, 2015) and co-occur or operate via similar mechanisms in hyper-tolerant species (Pallarés et al, 2016). These traits appear to have evolved multiple times across different lineages, but are generally associated with times of global aridification (Arribas et al, 2014).…”