A fruitful endeavor: scent cues and echolocation behavior used by Carollia castanea to find fruit

Animals rely on multiple sensory modalities to perform even the simplest ecological tasks (Burkhardt 1989; Siemers and Schnitzler 2000; Holland et al. 2005; Knaden and Graham 2016). One of the main goals of behavioral and sensory ecology lies in understanding the ability of different species to employ and modulate their sensory modes in the context of different environmental cues, and how the resulting behavioral decisions ultimately affect their ecology and evolution. Frugivores use various cues, including components of fruit color (Burkhardt 1989; Hiramatsu et al. 2008; Melin et al. 2008; Osorio and Vorobyev 2008; Valenta et al. 2013), shape (Von Helversen and Von Helversen 1999; Kalko and Condon 1998), and scent (Sanchez et al. 2006; Valenta et al. 2013) to find and select ripe fruit, and exhibit corresponding sensory specializations in their visual, auditory, and/or olfactory systems to target those cues (Catania 1999; Muller et al. 2007; Vanderelst et al. 2010). Little is known, however, about what scenarios facilitate or constrain sensory use and modulation during fruit location, selection, and acquisition in vertebrate frugivores. Insight into these processes would provide mechanistic understanding of the behaviors underlying their foraging ecology. Frugivorous and omnivorous Neotropical leaf-nosed bats (Phyllostomidae) use three major senses, echolocation, olfaction, and vision, for navigation and foraging (e.g., Reiger and Jakob 1988; Gutierrez et al. 2018; Thiele and Winter 2005; Kalko and Condon 1998), which makes these organisms an exceptional system for investigating the relative role of different sensory modes during ecologically important tasks. Although there has been some work on phyllostomid vision, including comparisons of their short- and long-wave opsins (Muller et al. 2007, 2009; Kries et al. 2018; Sadier et al. 2018; Gutierrez et al. 2018), the importance of vision in ripe fruit location and selection has not been experimentally tested in phyllostomids. By contrast, experimental evidence strongly suggests that omnivorous phyllostomids rely primarily on echolocation to locate fruits (Kalko and Condon 1998), and specialized frugivores employ either olfaction or a combination of olfaction and echolocation to locate ripe fruit (Kalko and Schnitzler 1993; Korine and Kalko 2005; Hodgkison et al. 2007, 2013). The relative importance of different sensory modes for fruit detection may depend on which plant cues can be readily perceived within a specific environmental context. To date, little is known about whether and how frugivorous phyllostomids integrate their primary sensory modes (echolocation and olfaction) conditional on which plant cues are present. While plant scents can travel over short or long distances (Riffell et al. 2014), they are rarely directional and may be difficult to detect in saturated scent environments such as rainforests. Conversely, echolocation allows for highly precise prey detection (Schnitzler and Kalko 2001; Brinklov et al. 2009; Jakobsen et al. 2013), but phyllostomids emit short, high frequency, and low intensity calls (Thies et al. 1998; Korine and Kalko 2005). The echoes from these calls provide information about size, shape, texture, range, and position of an object in space relative to the bat (Simmons et al. 1975, 1983; Simmons and Stein 1980; Neuweiler 1989; Schmidt et al. 2000; Schnitzler and Kalko 2001), but these types of information are only effective at very short distances because low intensity, high frequency calls attenuate rapidly in warm, humid environments (e.g., 45–90 kHz attenuate at 1.4–4 dB/m at 25°C and 80% humidity; Jakobsen et al. 2013). Additionally, surrounding foliage can produce acoustic masking effects that may complicate fruit detection (Arlettaz et al. 2001; Korine and Kalko 2005). Therefore, flexibility in olfaction versus echolocation use could be highly beneficial for frugivorous bats given the limitations of each sensory mode within complex forest environments. Here, we study the primary plant cues from vegetation and fruits and how they relate to the roles of echolocation and olfaction for fruit detection and localization in the chestnut short-tailed fruit bat, Carollia castanea, a highly abundant frugivore and ecologically important seed disperser that inhabits forests in Central and South America (Bonaccorso 1979; Fleming 1991; Fig. 1). This research builds upon the seminal work of Thies et al. (1998), which demonstrated the importance of olfaction for fruit detection in Carollia; here we investigate the relative contributions of vegetative and fruit scent cues that drive C. castanea’s foraging decisions, and how varying foraging scenarios (i.e., changing of plant scent cues) may affect the relative reliance of these bats on olfaction versus echolocation for fruit detection. Evaluating the effect of vegetative scents on frugivore foraging behavior is particularly important because background scents from neighboring plants can impact the ability of animals to discriminate fruit or flower odors (Riffell et al. 2014) or, if vegetative scents are from the same plant, they can amplify the scent of the food source and make it more potent (e.g., Raguso and Willis 2005; Rusch et al. 2016; Stutz et al. 2016; McArthur et al. 2019). Open in a separate window Fig. 1 Study organisms, Carollia castanea (left) and Piper sancti-felicis (right). Photo credit: S.E. Santana.