Salt has contrasting effects on the digestive processing of dilute nectar by two Neotropical nectarivorous bats

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Highlights

  • Both bat species did not present compensatory feeding.

  • Intake rate of 2.5 and 5% sucrose solutions supplied a fraction of the daily energy needs estimated for the bats.

  • Salt addition decreased the intake rate of 5% sugar solutions by Greater Antillean Long-tongued bat.

  • Salt addition increased the intake rate of 2.5 and 5% sugar solutions by the Brown flower bat.

Abstract

Nectarivorous vertebrates might include sugar-dilute nectar in their diet and they are expected to undergo compensatory feeding. However, physiological constraints might limit the intake of sugar-dilute nectar, affecting energy budgets. Among other physiological processes, the limiting role of osmoregulation is supported by enhanced intake rate of dilute sugar solutions by avian nectarivores when salt is added. We tested if the Greater Antillean Long-tongued bat (Monophyllus redmani) and the Brown flower bat (Erophylla sezekorni) compensated energy intake when fed dilute-sugar solutions (2.5 and 5% sucrose), and if salt content (11, 20 and 40 mM NaCl l−1) modulated the intake rate of these solutions. Both species were unable to compensate intake of solutions with varying sugar densities, and energy intake on the 2.5 and 5% diets was lower than on the most concentrated diets (10, 20 and 30% sucrose). Both species responded differently to the addition of salt. Salt addition did not affect the intake of 2.5% sugar solutions by the Greater Antillean Long-tongued bat, and it decreased the intake of 5% sugar solutions. In contrast, the Brown flower bat increased the intake of 2.5 and 5% sugar solutions when salt was added. Intake responses to varying sugar densities of our two focal species and that of other bat species previously studied indicate that they are not uniform and that they might be modulated by digestive and osmoregulatory physiological traits.

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 single bond 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 (8.5single bond34% 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 (3single bond5%) to sugar-rich (30single bond33%; 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 single bond .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.

References (40)

  • J. Ayala-Berdon et al.

    Seasonal intake responses in the nectar-feeding bat Glossophaga soricina

    J. Comp. Physiol. B.

    (2009)
  • H.G. Baker et al.

    Chemical constituents of nectar in relation to pollination mechanisms and phylogeny

  • G. Cassoti et al.

    Relationships between renal morphology and diet in 26 species of new World bats (suborder Microchiroptera)

    Zoology

    (2006)
  • A. Cirranello et al.

    Morphological diagnoses of higher-level phyllostomid taxa (Chiroptera: Phyllostomidae)

    Acta Chiropt.

    (2016)
  • I.F. Fishman

    Gustatory responses of a tropical frugivorous bat

    Proc. Iowa Acad. Sci.

    (1963)
  • P.A. Fleming et al.

    Osmoregulation in an avian nectarivore, the whitebellied sunbird Nectarinia talatala: response to extremes of diet concentration

    J. Exp. Biol.

    (2003)
  • P.A. Fleming et al.

    Concentration and temperature effects on sugar intake and preferences in a sunbird and a hummingbird

    Funct. Ecol.

    (2004)
  • T. Göttlinger et al.

    What do nectarivorous bats like? Nectar composition in Bromeliaceae with special emphasis on bat-pollinated species

    Front. Plant Sci.

    (2019)
  • B. Hartman Bakken et al.

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

    Am. J. Physiol. Ren. Physiol.

    (2008)
  • L.G. Herrera M. et al.

    Sucrose hydrolysis does not limit food intake by Pallas’s long-tongued bats

    Physiol. Biochem. Zool.

    (2008)
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