A Fruitful Endeavor: Scent Cues and Echolocation Behavior Used by Carollia castanea to Find Fruit

Abstract

Synopsis Frugivores have evolved sensory and behavioral adaptations that allow them to find ripe fruit effectively, but the relative importance of different senses in varying foraging scenarios is still poorly understood. Within Neotropical ecosystems, short-tailed fruit bats (Carollia: Phyllostomidae) are abundant nocturnal frugivores that rely primarily on Piper fruits as a food resource. Previous research has demonstrated that Carollia employs olfaction and echolocation to locate Piper fruit, but it is unknown how their sensory use and foraging decisions are influenced by the complex diversity of chemical cues that fruiting plants produce. Using free-ranging C. castanea and their preferred food, Piper sancti-felicis, we conducted behavioral experiments to test two main hypotheses: (1) foraging decisions in C. castanea are primarily driven by ripe fruit scent and secondarily by vegetation scent, and (2) C. castanea re-weights their sensory inputs to account for available environmental cues, with bats relying more heavily on echolocation in the absence of adequate scent cues. Our results suggest that C. castanea requires olfactory information and relies almost exclusively on ripe fruit scent to make foraging attempts. Piper sancti-felicis ripe fruit scent is chemically distinct from vegetation scent; it is dominated by 2-heptanol, which is absent from vegetation scent, and has a greater abundance of β-caryophyllene, β-ocimene, γ-elemene, and α-cubebene. Although variation in echolocation call parameters was independent of scent cue presence, bats emitted longer and more frequent echolocation calls in trials where fruit scent was absent. Altogether, these results highlight the adaptations and plasticity of the sensory system in neotropical fruit bats.

Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat

“…With this approach, instead of attempting to decode hundreds of receptors, 10-20 genes become good experimental candidates. For example, the Piper specialist C. castanea shows behavioral preference and attraction to volatile cues of ripened P. sancti-felicis fruits (Maynard et al 2019; Leiser-Miller et al 2020). Thus, a future study may test the hypothesis whether receptors demonstrating exceptional redundancy within C. castanea (e.g., such as those found in OR4 (Fig.…”

“…Second, behavioral assays have revealed that Carollia primarily use their sense of smell to initially locate fruiting patches and individual fruits, with echolocation being used at closer range to pinpoint the target fruit before grabbing it (Thies et al 1998). Carollia also only seems to perform feeding attempts in the presence of scent cues from Piper fruit (Thies et al 1998; Leiser-Miller et al 2020). Thus, Carollia ’s reliance on olfaction to locate Piper for fruits (and reciprocal reliance of Piper on chemical cues to attract Carollia for seed dispersal) makes it likely evolution has optimized the OR repertoires of each of these bat species for food detection.…”

Olfactory tracking strategies in a neotropical fruit bat

“…Like other neotropical leaf-nosed frugivores, Sturnira produces low-intensity, high-frequency echolocation calls, with peak frequencies ranging from 65 kHz to 92 kHz ( Jennings et al, 2004 ; Yoh et al, 2020 ), emitted via the nose. Fruit- and nectar-feeding bats within the family Phyllostomidae (including Sturnira ) are thought to primarily use echolocation for general orientation, as well as the final approach and selection of food items ( Gonzalez-Terrazas et al, 2016 ; Kalko and Condon, 1998 ; Leiser-Miller et al, 2020 ; Thies et al, 1998 ). We controlled for potential effects of echo-acoustic information during odor localization in Experiment 2.…”

“…Odor cues play a key role in foraging by frugivorous and nectarivorous bats ( Korine and Kalko, 2005 ; Rieger and Jakob, 1988 ; Thies et al, 1998 ; Von Helversen et al, 2000 ), but the extent to which bats rely upon olfaction to find food is still unknown. Olfaction was shown to be an important cue for detecting the presence of ripe fruit ( Leiser-Miller et al, 2020 ; Thies et al, 1998 ). Neotropical fruit bats are highly sensitive to fruit odors and can discriminate odor qualities and quantities – the first step in being able to recognize a concentration gradient ( Laska, 1990a , b ).…”

Fruit odorants mediate co-specialization in a multispecies plant–animal mutualism

“…These consisted of unripe P. sancti-felicis fruit (control) or unripe P. sancti-felicis fruit with either 2-heptanol, α-caryophyllene or α-phellandrene in the same concentrations and emission rates they are found in ripe fruit. These VOCs were selected because they are abundant and common in ripe fruit scent across all the Piper species studied (α-caryophyllene and α-phellandrene), or relatively rare but characteristic of P. sancti-felicis ripe fruit scent (2-heptanol; [24]; electronic supplementary material, data file S1). Samples were placed on 50 ml Falcon tubes, 40 cm apart, on a custom-built platform (see electronic supplementary materials for details).…”