Comparative aspects of natriuretic peptide physiology in non-mammalian vertebrates: a review

The natriuretic peptide system is a complex family of peptides and receptors that is primarily linked to the maintenance of osmotic and cardiovascular homeostasis. A natriuretic peptide system is present in each vertebrate class but there are varying degrees of complexity in the system. In agnathans and chondrichthyians, only one natriuretic peptide has been identified, while new data has revealed that multiple types of natriuretic peptides are present in bony fish. However, it seems in tetrapods that there has been a reduction in the number of natriuretic peptide genes, such that only three natriuretic peptides are present in mammals. The peptides act via a family of guanylyl cyclase receptors to generate the second messenger cGMP, which  mediates a range of physiological effects at key targets such as the gills, kidney and the cardiovascular system. This review summarises the current knowledge of the natriuretic peptide system in non-mammalian vertebrates and discusses the physiological actions of the peptides.

Performance of tropical fish recruiting to temperate habitats: role of ambient temperature and implications of climate change

The warming of coastal oceans due to climate change is increasing the overwinter survival of tropical fishes transported to temperate latitudes by ocean currents. However, the processes governing early post-arrival mortality are complex and can result in minimum threshold temperatures for overwinter survival, which are greater than those predicted based upon physiological temperature tolerances alone. This 3.5 mo laboratory study monitored the early performance of a tropical damselfish Abudefduf vaigiensis that occurs commonly during austral summer along the SE Australian coast, under nominal summer and winter water temperatures, and compares results with a co-occurring year-round resident of the same family, Parma microlepis. Survivorship, feeding rate, growth and burst swimming ability (as a measure of predator escape ability) were all reduced for the tropical species at winter water temperatures compared to those in summer, whereas the temperate species experienced no mortality and only feeding rate was reduced at colder temperatures. These results suggest that observed minimum threshold survival temperatures may be greater than predicted by physiology alone, due to lowered food intake combined with increased predation risk (a longer time at vulnerable sizes and reduced escape ability). Overwinter survival is a significant hurdle in pole-ward range expansions of tropical fishes, and a better understanding of its complex processes will allow for more accurate predictions of changes in biodiversity as coastal ocean temperatures continue to increase due to climate change.

Mechanisms for climate-induced mortality of fish populations in whole-lake experiments

The effects of climate change on plant and animal populations are widespread and documented for many species in many areas of the world. However, projections of climate impacts will require a better mechanistic understanding of ecological and behavioral responses to climate change and climate variation. For vertebrate animals, there is an absence of whole-system manipulative experiments that express natural variation in predator and prey behaviors. Here we investigate the effect of elevated water temperature on the physiology, behavior, growth, and survival of fish populations in a multiple whole-lake experiment, by using 17 lake-years of data collected over 2 years with differing average temperatures. We found that elevated temperatures in excess of the optimum reduced the scope for growth through reduced maximum consumption and increased metabolism in young rainbow trout, Oncorhynchus mykiss. Increased metabolism at high temperatures resulted in increased feeding activity (consumption) by individuals to compensate and maintain growth rates similar to that observed at cooler (optimum) temperatures. However, greater feeding activity rates resulted in greater vulnerability to predators that reduced survival to only half that of the cooler year. Our work therefore identifies temperature-dependent physiology and compensatory feeding behavior as proximate mechanisms for substantial climate-induced mortality in fish populations at the scale of entire populations and waterbodies.

Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in young fish cohorts

Given limited food, prey fishes in a temperate climate must take risks to acquire sufficient reserves for winter and/or to outgrow vulnerability to predation. However, how can we distinguish which selective pressure promotes risk-taking when larger body size is always beneficial? To address this question, we examined patterns of energy allocation in populations of age-0 trout to determine if greater risk-taking corresponds with energy allocation to lipids or to somatic growth. Trout achieved maximum growth rates in all lakes and allocated nearly all of their acquired energy to somatic growth when small in early summer. However, trout in low-food lakes took greater risks to achieve this maximal growth, and therefore incurred high mortality. By late summer, age-0 trout allocated considerable energy to lipids and used previously risky habitats in all lakes. These results indicate that: (i) the size-dependent risk of predation (which is independent of behaviour) promotes risk-taking behaviour of age-0 trout to increase growth and minimize time spent in vulnerable sizes; and (ii) the physiology of energy allocation and behaviour interact to mediate growth/mortality trade-offs for young animals at risk of predation and starvation.

Development and physiology of gastric dilation air sacculitis in Chinook salmon, Oncorhynchus tshawytscha (Walbaum)

The syndrome known as gastric dilation air sacculitis (GDAS) has previously been shown to affect Chinook salmon, Oncorhynchus tshawytscha, in seawater (SW) aquaculture. Feed and osmoregulatory stress have been implicated as potential epidemiological co-factors. The development and physiology of GDAS was investigated in SW and freshwater (FW) adapted smolts. Diet A (low-cohesion pellets) and diet B (high-cohesion pellets) were fed to both FW- and SW-adapted fish. GDAS was induced only in the SW trial on feeding diet A. Stimulated gastro-intestinal (GI) smooth muscle contractility, and fluid transport by the pyloric caeca were different in GDAS-affected fish, which also showed osmoregulatory dysfunction. Cardiac stomach (CS) smooth muscle contractility in response to acetylcholine and potassium chloride (KCl) was significantly reduced in fish fed diet A relative to controls from weeks 3–5. In contrast, maximal pyloric sphincter (PS) circular smooth muscle contraction in response to KCl was significantly elevated in fish fed diet A in weeks 4 and 5. Serum osmolality was elevated in GDAS-affected fish from week 2 of the SW trial. Fluid transport from the mucosal to serosal surface of isolated pyloric caeca was significantly reduced in weeks 3, 4 and 5 in SW fish fed diet A. Gastric evacuation from the stomach of healthy fish was shown to be significantly different when diets of low- and high-cohesion were fed. The results are consistent with the intestinal brake playing a role in the development of the disease.

Developmental stress can uncouple relationships between physiology and behaviour

Phenotypic correlations (rP) have frequently been observed between physiological and behavioural traits, and the nature of these associations has been shown to be modulated by a range of environmental stressors. Studies to date have examined the effects of acute stressors on physiology-behaviour interrelations, but the potential for permanent changes induced by exposure to stress during development remains unexplored. We exposed female zebra finches to dietary restriction during the nestling stage and tested how this affected rP among a variety of physiological traits (haematocrit, stress-induced corticosterone level and basal metabolic rate (BMR)) and behavioural traits (activity and feeding rates in novel and familiar environments). Developmental stress completely uncoupled the relationship between activity in a novel environment and two physiological traits: haematocrit and BMR. This suggests that nutritionally based developmental stress has provoked changes in the energy budget that alleviate the trade-off between maintenance (BMR) and locomotor activities.

Individual boldness traits influenced by temperature in male Siamese fighting fish.

Temperature has profound effects on physiology of ectothermic animals. However, the effects on temperature variation on behavioral traits are poorly studied in contrast to physiological endpoints. This may be important as even small differences in temperatures have large effects on physiological rates including overall metabolism, and behavior is known to be linked to metabolism at least in part. The primary aim of this study was to determine the effects of ambient temperature on boldness responses of a species of fish commonly used in behavioral experiments, the Siamese fighting fish (Betta splendens). At 26°C, subjects were first examined for baseline behaviors over three days, using three different (but complementary) 'open field' type assays tested in a fixed order. Those same fish were next exposed to either the same temperature (26°C) or a higher temperature (30°C) for 10days, and then the same behavioral assays were repeated. Those individuals exposed to increased temperatures reduced their latency to leave the release area (area I), spent more time in area III (farthest from release area), and were more active overall; together we infer these behaviors to reflect an increase in general 'boldness' with increased temperature. Our results add to a limited number of studies of temperature effects on behavioral tendencies in ectotherms that are evident even after some considerable acclimation. From a methodological perspective, our results indicate careful temperature control is needed when studying behavior in this and other species of fish.