The integration of osmoregulation and energy balance in nectar-feeding birds

Abstract

Nectar-feeding birds must ingest copious amounts of water due to their liquid diet. Large volumes of preformed water in the dilute diet mean that birds feeding on these diets risk the loss of solutes in order to excrete this water. Previous studies have found that on dilute diets (<0.25 mol.l-1), white-bellied sunbirds (Cinnyris talatala) are unable to maintain energy balance and lose excessive amounts of electrolytes via cloacal fluid. Therefore how these small nectarivores handle water and electrolytes is intricately linked with how they obtain energy from a nectar diet. Understanding the physiological mechanisms for handling water and electrolytes will reveal how nectarivorous birds can deal with a range of nectar diet concentrations. These mechanisms were investigated through a series of experiments that exposed birds to varying electrolyte and water loads through compensatory feeding (requiring birds to ingest greater volumes of energy-dilute diets than energy-concentrated diets). I tested the effect of adding electrolytes to a 0.1 mol.l-1 sucrose diet in white-bellied sunbirds (Cinnyris talatala) and New Holland honeyeaters (Phylidonyris novaehollandiae). Addition of salts (NaCl and KCl) enabled both species to drink significantly more of the dilute diet than in the absence of salt. On 20 mmol.l-1 combined salts, both sunbirds and honeyeaters consumed an extraordinary 8 times their body mass in fluid daily. KCl alone had no effect on consumption but a loss of Na+ clearly limits consumption of extremely dilute diets. Plasma Na+ levels, and sucrose assimilation efficiencies confirmed this, leading to the conclusion that Na+ depletion on very dilute salt-free diets interferes with water excretion or sugar digestion and/or assimilation. I then evaluated the behavioural responses of these two nectarivore species to salt solutions. Preference tests (simultaneously presenting birds with a range of diets with salt added and repeating this experiment with different sugar concentration base solutions) showed that both species ingested similar amounts of all diets when fed the concentrated base solutions (i.e. low total intake). However, when the birds had to increase their intake of more dilute sucrose diets to maintain energy balance, they avoided the higher salt concentrations. Through active diet switching, birds maintained constant intakes of both sucrose and sodium. To test renal concentrating abilities of these two nectarivores, I conducted no choice tests, by feeding them 0.63 mol.l-1 sucrose containing 5-200 mmol.l-1 NaCl over a 4 h trial. In both species, cloacal fluid osmolalities increased with diet NaCl concentration, but while sunbirds excreted all the Na+ ingested, honeyeaters retained sodium on the more concentrated diets. The kidneys of sunbirds and honeyeaters, like those of hummingbirds, are well suited to diluting urine; however unlike hummingbirds, sunbirds and honeyeaters also appear to concentrate urine efficiently when necessary. The final part of this thesis examined how these birds deal with excess preformed water loads on dilute nectar diets. I used the elimination of intramuscular-injected [14C]-L-glucose and 3H2O to quantify intestinal and renal water handling on diets varying in sugar concentration. Both species showed significant modulation of intestinal water absorption, allowing excess water to be shunted through the intestine on dilute diets and therefore reducing renal load. During the natural overnight fast, both sunbirds and honeyeaters arrested whole kidney function, shutting down GFR as another way of reducing renal load. Both sunbirds and honeyeaters are able to maintain osmotic balance on markedly different diet concentrations and hence preformed water loads, by varying intestinal water absorption as well as excretion via the intestine and kidneys.