Maternal Mouth-To-Mouth Feeding Behaviour in Flower-Visiting Bats, But
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Behavioural Processes 165 (2019) 29–35 Contents lists available at ScienceDirect Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc Maternal mouth-to-mouth feeding behaviour in flower-visiting bats, but no experimental evidence for transmitted dietary preferences T ⁎ Andreas Rosea, , Saskia Wöhlb,c, Jan Bechlera, Marco Tschapkaa,d, Mirjam Knörnschildd,e,f a Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert-Einstein Allee 11, D-89069, Ulm, Germany b Institute of Zoology, University of Erlangen-Nuremberg, Staudtstr. 5, 91058, Erlangen, Germany c Dienstleistungszentrum Ländlicher Raum Westerwald-Osteifel, Fachzentrum für Bienen und Imkerei, Im Bannen 38, 56727, Mayen, Germany d Smithsonian Tropical Research Institute, Building 401 Tupper, Luis Clement Avenue, Balboa Ancon, Panama e Animal Behavior Lab, Free University Berlin, Takustrasse 6, 14195, Berlin, Germany f Museum für Naturkunde - Leibniz Institute for Evolution and Biodiversity Science, Invalidenstraße 43, 10115, Berlin, Germany ARTICLE INFO ABSTRACT Keywords: In addition to breast milk, several mammals feed their offspring with primary food items. This provisioning can Choice experiment offer both energetic and informational benefits: young might use parentally provided food as a source of nu- Glossophaga soricina trients, but also as a valuable option to socially learn about adults’ food. For bats, there are only very few and Maternal food provisioning partially anecdotal reports of adults feeding their pups with primary food, and there is also a lack of information Nectar flavour about social learning processes during ontogeny. In the present study, we provide experimental evidence that Parental care lactating flower-visiting bats (Glossophaga soricina) provide regurgitated nectar via mouth-to-mouth feeding Social learning behaviour to their pups. After licking at their mothers’ slightly opened mouth, pups defecated a marker sub- stance that was exclusively available in the mothers’ nectar diet. We additionally investigated associated in- formational benefits by testing for a social transmission of dietary preferences. We experimentally induced a dietary preference for specifically flavoured nectars to mothers with non-volant pups. Subsequently, after pups became volant, we tested their dietary preferences in a choice experiment. However, we found no experimental evidence that pups adopted the preferences of their mothers. 1. Introduction There is only very little knowledge about parental provisioning of primary food in bats. Even though all bats exhibit a distinct parental In addition to breastfeeding, several mammals exhibit behavioural care (Kunz and Hood, 2000), sharing of primary food items has only capabilities to additionally feed their young with primary food items been observed in very few animal-eating and frugivorous species, and (e.g. Brown et al., 1983; Holekamp and Smale, 1990; Jaeggi et al., most of these observations remained anecdotal (e.g. Brown et al., 1983; 2008). While the provisioning using maternal nutrient reserves via Pierson and Rainey, 1992; Altringham, 1996; Wilkinson and breast milk enables mothers to provision young even when food sup- Boughman, 1999). Food items are provided mouth-to-mouth in these plies are unreliable, a provisioning with primary food items is argued to species; predatory bats deliver solid prey items like small vertebrates or be more energy efficient at delivering nutrients to the offspring (Dall insects to their pups (e.g. Raghuram and Marimuhtu 2007; Geipel et al., and Boyd, 2004). 2013), while pups of vampire bats (Desmodus rotundus, Diphylla ecau- Moreover, parental provisioning with primary food items might data) lick regurgitated blood out of the adults’ mouth (Schmidt, 1978; carry additional benefits, such as facilitated development of food- Delpietro and Russo, 2002). Potential informational benefits of mouth- handling skills or even a transmission of foraging related information to-mouth feeding behaviour in bats were discussed, but have not been from parents to offspring. Juveniles might socially learn about their tested yet (Geipel et al., 2013). parents’ dietary preferences or the characteristics of adults’ food in While adult individuals in many bat species use social information general, for example helping them to discriminate palatable from toxic when making foraging decisions (horizontal social learning; Hoppitt food when foraging alone (informational hypotheses, Brown et al., and Laland, 2013; bats: e.g., Ratcliffe and ter Hofstede, 2005; Wright 2004; Jaeggi et al., 2008; Thornton, 2008). et al., 2011; O’Mara et al., 2014; Rose et al., 2016), we know very little ⁎ Corresponding author. E-mail address: [email protected] (A. Rose). https://doi.org/10.1016/j.beproc.2019.06.001 Received 26 November 2018; Received in revised form 26 April 2019; Accepted 1 June 2019 Available online 04 June 2019 0376-6357/ © 2019 Elsevier B.V. All rights reserved. A. Rose, et al. Behavioural Processes 165 (2019) 29–35 about social learning processes during juvenile development (vertical social learning; Ganesh et al., 2016; Wright, 2016). Comparable to other mammals, an early contact with food cues via mouth-licking (cf. McFadyen-Ketchum and Porter, 1989) or even via direct provisioning (cf. Thornton, 2008) should be a valuable option for bat pups to gain information about adults’ food and enable them to adopt their parents’ dietary preferences. Pallas’ long-tongued bat (Glossophaga soricina) is a medium sized flower-visiting bat of ca. 10 g, inhabiting tropical habitats from Mexico to Argentina (Alvarez et al., 1991). Its diet mainly consists of nectar and pollen from flowers of a variety of different bat-pollinated plants, which partially share distinct chiropterophilous characteristics, including an unpleasant, garlic-like scent based on sulphur-containing compounds (Heithaus et al., 1975; Knudsen and Tollsten, 1995; Tschapka and Dressler, 2002), which are also flavouring the nectar of some species (Raguso, 2004). While feeding, bats perform hovering flights in front of these flowers and lick up nectar using their elongated tongue (e.g. Harper et al., 2013). Females give birth to a single pup that is nursed with breast milk for about two months (Alvarez et al., 1991; Pink, 1996; Engler et al., 2017). Pups start becoming volant at an age of about 20 to 25 days, but like in other bat species, first flights are short and per- formed clumsily for at least another week (Pink, 1996). Flower-visiting bats (Phyllostomidae: Glossophaginae) have not been reported to in- corporate sharing of primary food into parental care so far, but nursing pups of G. soricina were observed to perform a licking behaviour at their Fig. 1. Mouth-to-mouth feeding behaviour. Pup (left) feeds on regurgitated mothers’ mouth. This behaviour, which was observed to start at a pup nectar out of the slightly opened mouth of its mother (right). age of 9 to 12 days and interpreted as feeding behaviour by Pink (1996), appears comparable to the behaviour of vampire bat pups when vertical social learning of dietary preferences was investigated in free fed by adults with regurgitated blood (Wilkinson, 1990). living G. soricina in the Santa Rosa National Park, Costa Rica (UTM: In the present study, we tested the hypothesis that the pups’ licking 16 P 651,137 1,198,498). Over two reproductive periods, we caught 16 behaviour at their mothers’ mouth represents a mouth-to-mouth mother-pup-pairs that were split into two experimental groups and kept feeding behaviour and thus maternal provisioning of floral nectar. We separated in flight cages. further investigated the possibility that this behaviour might not only For a period of 18.2 ( ± 6.4 SD) days during which pups were still provide nutrients to G. soricina pups, but also information about food non-volant, we artificially induced different dietary preferences to sources and their mothers’ dietary preferences. We hypothesized that mothers of each group by allowing them to feed ad libitum on only one pups would adopt the dietary preferences of their mothers. Such a of two different-flavoured artificial nectars from an artificial flower vertical social transmission of dietary preferences could help pups to (flavoured period; group 1: strawberry flavour; group 2: chocolate fla- learn about the characteristics of palatable food, for example by getting vour). Both flavoured nectar types were easily distinguishable by the familiarized with the scent and taste of bat-pollinated flowers. human nose and mouth. Pups were unable to fly during the whole flavoured period and solely fed by their mothers with breast milk, and 2. Materials and methods with nectar during mouth-to-mouth feeding behaviour. Once pups became volant (indicated by the onset of first, clumsy 2.1. Verification of nectar transfer via mouth-to-mouth feeding behaviour flights) and thus had potentially access to nectar on their own, we stopped flavouring the nectar to prevent them from becoming ac- The potential mouth-to-mouth feeding behaviour was experimen- quainted with our experimentally flavoured nectar without being fed tally investigated in captive G. soricina at the University of Erlangen- with it by their mothers. During this unflavoured period of 12.3 Nuremberg. Once pups’ licking behaviour at their mothers’ mouth was ( ± 4.8) days, pups learned to perform hovering flights and to feed from observed for the first time during ontogeny (Fig. 1), we started a ver- the artificial flower by themselves (Table 1). Even though this in-