Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Salt has contrasting effects on the digestive processing of dilute nectar by two Neotropical nectarivorous bats
Graphical abstract
Introduction
Some nectarivorous vertebrates forage on flowers producing sugar-dilute nectar (Baker and Baker, 1982; Nicolson, 2002). Consequently, it is expected that nectarivores will increase their food intake to compensate for low energy content maintaining energy balance (Martínez del Rio et al., 2001). However, compensating food intake is not trivial because several factors might constrain food ingestion rate, such as the limits imposed by the size of the gut, the rate of sugar assimilation, kidney processing rates, and the cost of warming food to body temperature (Nicolson and Fleming, 2003). In addition, due to the watery nature of floral nectar, over ingestion of water on sugar-dilute food may represent an osmoregulatory challenge for the animal (Martínez del Rio et al., 2001; Hartman Bakken et al., 2008). For example, electrolyte loss increases when nectarivores are fed dilute nectar (Fleming and Nicolson, 2003).
The limiting role of osmoregulation in compensatory feeding is supported by recent studies showing that some nectarivores increase their intake rate of dilute nectar when salt is added. For instance, intake rate of dilute sucrose solution (2.5 3.4% w/w) by Whitebellied sunbirds (Cinnyris talatala), New Holland honeyeaters (Phylidonyris novaehollandiae) and Red-legged Honeycreepers (Cyanerpes cyaneus) was higher when salt was added than in salt-free sucrose solutions (Purchase et al., 2010, Purchase et al., 2013; Mancina and Herrera M., 2016). Furthermore, Whitebellied sunbirds and New Holland honeyeaters had similar energy intake on sugar-dilute nectar (3.4% w/w) with salt as on salt-free solutions with higher sugar concentrations (8.534% w/w). Those investigations have proved that compensatory feeding may be influenced by salt intake (Purchase et al., 2010). Among mammals, the osmoregulatory effect on the intake of dilute nectar has been tested only for the Egyptian fruit bat (Rousettus aegyptiacus; Herrera M. et al., 2015). In contrast to nectarivorous birds, Egyptian fruit bats do not increase intake rates of dilute nectar (7% w/w) when salt is added, suggesting that osmoregulation might not have the same effect on the intake rate of nectarivores of different taxa.
Flowers visited by Neotropical nectarivorous bats produce nectar with a broad range of sugar and ion concentrations. Nectars used by these bats range from sugar-dilute (35%) to sugar-rich (3033%; von Helversen, 1993; Winter and von Helversen, 2001; Rodríguez-Peña et al., 2016a), with variable levels of cations (1.9 mMol l−1 to 22.5 mMol l−1; Göttlinger et al., 2019) and anions (0.7 mMol l−1 to 11.9 mMol l−1; Göttlinger et al., 2019). New World nectarivorous bats are represented by two subfamilies: Glossophaginae and Lonchophyllinae (Cirranello et al., 2016). Compensatory feeding has been tested only in glossophagine species belonging to the tribes Glossophagini and Choeronycterini with contrasting results. Intake of dilute nectar is limited in some bat species (Ramírez et al., 2005; Ayala-Berdon et al., 2008, Ayala-Berdon et al., 2009, Ayala-Berdon et al., 2011, Ayala-Berdon et al., 2013; Herrera M. and Mancina G., 2008), but species that live in environments at higher altitudes and colder temperatures show compensatory feeding (Ayala-Berdon and Schondube, 2011; Ayala-Berdon et al., 2013, Ayala-Berdon et al., 2018; Cruzblanca-Castro et al., 2018). We examined intake rate of solutions with varying sugar densities and the effect of salt content on the intake of dilute sugar solutions in glossophagine species belonging to the tribes Glossophagini and Brachyphyllini: the Greater Antillean Long-tongued bat (Monophyllus redmani) and the Brown flower bat (Erophylla sezekorni), respectively. These species are endemic to the Greater Antilles and they feed on nectar, pollen, fruits and insects (Soto-Centeno and Kurta, 2006; Mancina et al., 2007). We tested the hypothesis that, similarly to lowland glossophagines (Ramírez et al., 2005; Ayala-Berdon et al., 2008, Ayala-Berdon et al., 2009, Ayala-Berdon et al., 2011, Ayala-Berdon et al., 2013; Herrera M. and Mancina G., 2008), the Greater Antillean Long-tongued bat and the Brown flower bat do not show compensatory feeding, and that their intake of sugar-dilute solutions is modulated by osmoregulatory constraints.
Section snippets
Animal capture and husbandry
This study was conducted with adult, non-reproductive male individuals of the Greater Antillean Long-tongued bat (10.6 ± 0.09 g; mean ± SE) and the Brown flower bat (14.2 ± 0.12 g) captured in La Virgen cave (23°01′N and 82°06′W) in the Siboney-Juticí Ecological Reserve, Santiago de Cuba, Cuba. The cave was visited several times during November 2016 and January 2017 to capture sets of different individuals of both bat species. Colony sizes of each bat species in this cave were of several
Food intake of sugar-only diets
Food intake of unsalted solutions by the Greater Antillean Long-tongued bat increased as sugar concentration decreased (F4, 39 = 20.78, P < .0001): intakes of the two most dilute diets (2.5 and 5%) were higher than those of the other diets (10, 20 and 30%; Ps = .0001 .01; Fig. 1A), and intake of the 10% diet was higher than that of the 30% diet (P = .008). The amount of energy ingested varied significantly with sugar concentration (F4, 39 = 25.47, P < .0001): energy intake rates of bats
Compensatory feeding
Neotropical nectarivorous bats feed on flowers that produce nectar with different sugar densities, including very dilute sugar solutions (2.8%10% w/w; Sazima et al., 1989, Sazima et al., 1999; Tschapka and von Helversen, 1999; Martén-Rodríguez and Fenster, 2008; Lovig, 2013; Rodríguez-Peña et al., 2016a). Food intake by the Greater Antillean Long-tongued bat and the Brown flower bat increased as dietary sugar content decreased, and it was equivalent to 3.3 and 2.0 fold of their body mass,
Acknowledgements
The study was funded by Consejo Nacional de Ciencia y Tecnología with a research grant (#43343) to LGHM. All animal care procedures and experimental protocols adhered to institutional regulations of the Instituto de Ecología y Sistemática. T. H. Fleming and K. C. Welch Jr., and three anonymous reviewers kindly helped with the preparation of the manuscript.
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