A nectar-feeding mammal avoids body fluid disturbances by varying renal function

Abstract

To maintain water and electrolyte balance, nectar-feeding vertebrates oscillate between two extremes: avoiding overhydration when feeding and preventing dehydration during fasts. Several studies have examined how birds resolve this osmoregulatory dilemma, but no data are available for nectar-feeding mammals. In this article, we 1) estimated the ability of Pallas's long-tongued bats (Glossophaga soricina; Phyllostomidae) to dilute and concentrate urine and 2) examined how water intake affected the processes that these bats use to maintain water balance. Total urine osmolality in water- and salt-loaded bats ranged between 31 +/- 37 mosmol/kgH(2)O (n = 6) and 578 +/- 56 mosmol/kgH(2)O (n = 2), respectively. Fractional water absorption in the gastrointestinal tract was not affected by water intake rate. As a result, water flux, body water turnover, and renal water load all increased with increasing water intake. Despite these relationships, glomerular filtration rate (GFR) was not responsive to water loading. To eliminate excess water, Pallas's long-tongued bats increased water excretion rate by reducing fractional renal water reabsorption. We also found that rates of total evaporative water loss increased with increasing water intake. During their natural daytime fast, mean GFR in Pallas's long-tongued bats was 0.37 ml/h (n = 10). This is approximately 90% lower than the GFR we measured in fed bats. Our findings 1) suggest that Pallas's long-tongued bats do not have an exceptional urine-diluting or -concentrating ability and 2) demonstrate that the bats eliminate excess ingested water by reducing renal water reabsorption and limit urinary water loss during fasting periods by reducing GFR.

Fig. 1.

Data from Pallas's long-tongued bats (Glossophaga soricina) illustrating: 1) our protocol in experiment 2 and 2) that the appearance of ³H₂O (•, solid lines) and l-[¹⁴C]-labeled glucose (○, dashed lines) in urine over time follows single-compartment, first-order kinetics. Each panel (A–C) shows data for an individual bat. For each marker elimination curve, numerical values represent the coefficient of determination (r²). ³H and ¹⁴C concentrations in urine are log_e transformed here for clarity; however, we determined r² values and performed our analyses on nontransformed data (38). dpm, disintegrations per minute.

Fig. 2.

The influence of water intake rate on water budget components in Pallas's long-tongued bats (Glossophaga soricina) during both the early morning (○, dashed lines) and late evening (•, solid lines). Water flux increased linearly with water intake (A). Fractional water absorption in the gastrointestinal tract (f_A) was independent of water intake (B). Hourly rates of both fractional body water turnover (f_T; C) and renal water load (D) increased linearly with water intake. During the early morning, glomerular filtration rate (GFR) was independent of water intake; during the late evening, however, GFR increased linearly with water intake (E). Fractional water reabsorption in the kidney (f_R) decreased linearly with water intake during the early morning (F). Also during the early morning, both the rate of water excretion (G) and our indirect estimate of total evaporative water loss (TEWL′; H) increased linearly with water intake. The assumption of neutral water balance was not met for bats during the late evening measurement period.

Fig. 3.

GFR during dissimilar times of day in Pallas's long-tongued bats (Glossophaga soricina). Our GFR and mean GFR (GFR′) estimates (open bars) were all lower than the allometric prediction of 6.06 ml/h (solid bar; see Ref. 45). GFR during the early morning and late evening feeding periods was 3.46 ± 1.43 (n = 10) and 2.69 ± 2.09 ml/h (n = 10), respectively. Some of the variability in late evening GFR is explained by the positive and linear relationship between GFR and water intake during this period (Fig. 2E). GFR′ during the day, when bats were naturally fasted, was 0.37 ± 0.20 ml/h (n = 10). Values are means ± SD; lowercase letters denote statistical differences.