Echolocation in Oilbirds and swiftlets

Abstract

The discovery of ultrasonic bat echolocation prompted a wide search for other animal biosonar systems, which yielded, among few others, two avian groups. One, the South American Oilbird (Steatornis caripensis: Caprimulgiformes), is nocturnal and eats fruit. The other is a selection of diurnal, insect-eating swiftlets (species in the genera Aerodramus and Collocalia: Apodidae) from across the Indo-Pacific. Bird echolocation is restricted to lower frequencies audible to humans, implying a system of poorer resolution than the ultrasonic (>20 kHz) biosonar of most bats and toothed whales. As such, bird echolocation has been labeled crude or rudimentary. Yet, echolocation is found in at least 16 extant bird species and has evolved several times in avian lineages. Birds use their syringes to produce broadband click-type biosonar signals that allow them to nest in dark caves and tunnels, probably with less predation pressure. There are ongoing discrepancies about several details of bird echolocation, from signal design to the question about whether echolocation is used during foraging. It remains to be seen if bird echolocation is as sophisticated as that of tongue-clicking rousette bats. Bird echolocation performance appears to be superior to that of blind humans using signals of notable similarity. However, no apparent specializations have been found so far in the birds' auditory system (from middle ear to higher processing centers). The advent of light-weight recording equipment and custom software for examining signals and reconstructing flight paths now provides the potential to study the echolocation behavior of birds in more detail and resolve such issues.

Keywords: Aerodramus; Collocalia; Oilbird; Steatornis caripensis; biosonar; click; echolocation; swiftlets.

Figure 1

Composite phylogeny based on three separate studies showing relationships between (A) Apodiformes (hummingbirds and swifts—purple) and Caprimulgiformes (nightjars and allies—green) (Hackett et al., 2008), (B) swifts (Apodidae) (Päckert et al., 2012), and (C) swiftlets (Collocallini, blue) (Thomassen et al., 2005). Swiftlets are monophyletic and comprise three genera: Aerodramus spp., Hydrochous gigas, and Collocalia spp. (Thomassen et al., 2005). Twenty-six swiftlet species are currently recognized (Chantler et al., ; Thomassen, 2005). Nine species (A. brevirostris, A. hirundinaceus, A. infuscatus, A. inquietus, A. leucophaeus, A. nuditarsus, A. orientalis, A. papuensis, and A. unicolor) were not included in the shown phylogeny and the placement of A. fuciphagus^* and A. vanikorensis^** was ambiguous. Echolocating species appear in bold. Echolocation has been confirmed for 16 swiftlet species; H. gigas, C. esculenta and C. linchi do not echolocate. Echolocation abilities of remaining species are uncertain. Photographs by Signe Brinkløv: (A) Oilbirds (Steatornis caripensis) photographed on nest at Dunstan's Cave, Asa Wright Nature Centre, Trinidad (2012), (C) Indian Swiftlets (Aerodramus unicolor) photographed on nest in a railway tunnel near Pattipola, Sri Lanka (2012).

Figure 2

Composite waveform (top) and spectrogram (bottom) of echolocation signals from 6 vertebrate species: common bottlenose dolphin (Tursiops truncatus), sample rate (fs) = 500 kHz; laryngeal echolocating bat (Eptesicus fuscus), fs = 250 kHz; tongue-clicking pteropodid bat (Rousettus aegyptiacus), fs = 250 kHz; Oilbird (Steatornis caripensis), fs = 75 kHz; swiftlet (Aerodramus unicolor), fs = 250 kHz and echolocating blind human subject (Homo sapiens), fs = 48 kHz. Top inserts both have total time scales of 300 ms and illustrate the double clicks often emitted by echolocating Rousettus spp. and most echolocating swiftlet species. Bat and bird recordings made by Signe Brinkløv, dolphin recording courtesy of Magnus Wahlberg, human recording courtesy of Cynthia Moss. Spectrograms were created in BatSound v. 4 using an FFT size of 256, except for those from R. aegyptiacus and S. caripensis, for which an FFT size of 128 was used. All spectrograms were made using 98% overlap. Colors indicates relative amplitude going from low (light color) to high (darker color). Note the interrupted frequency scale between 100 and 230 kHz. Waveform amplitudes have all been normalized to the same level.

Figure 3

Comparative audiograms for 5 vertebrates, all of which are capable of some form of echolocation. Audiograms shown are visually estimated averages derived from previous experiments with Oilbirds (Steatornis caripensis) (Konishi and Knudsen, 1979), one swiftlet species (Aerodramus spodiopygia) (Coles et al., 1987), one tongue-clicking pteropodid bat species (Rousettus aegyptiacus) (Koay et al., 1998), one laryngeal echolocating bat species (Eptesicus fuscus) (Koay et al., 1997) and humans (Homo sapiens) (Jackson et al., 1999). Audiograms of R. aegyptiacus, E. fuscus and H. sapiens were obtained from behavioral experiments, whereas thresholds from S. caripensis and A. spodiopygia were based on neurophysiological data from anaesthized birds. Note that relative threshold differences should not be directly compared due to differences in experimental conditions, e.g., different ambient noise levels. Colored blocks correspond to the frequency range where echolocation signals of each group have most energy (measured as −15 dB bandwidth—frequency range 15 dB down from either side of the spectrum peak—of a single click per species), for example the red block is the −15 dB bandwidth of a R. aegyptiacus click. The recording used for bandwidth measurements of human echolocation clicks was provided by C. Moss and the −15 dB bandwidth of A. spodiopygia was estimated from Figure 3B in Coles et al. (1987). Remaining bandwidths were measured from recordings made by Signe Brinkløv.